diff --git a/entitlements/entitlements.go b/entitlements/entitlements.go
index e524b3037f0da..63ca0f5b6e066 100644
--- a/entitlements/entitlements.go
+++ b/entitlements/entitlements.go
@@ -16,6 +16,8 @@
 
 package entitlements
 
+import "github.com/gravitational/teleport/api/client/proto"
+
 type EntitlementKind string
 
 // The EntitlementKind list should be 1:1 with the Features & FeatureStrings in salescenter/product/product.go,
@@ -57,3 +59,67 @@ var AllEntitlements = []EntitlementKind{
 	ExternalAuditStorage, FeatureHiding, HSM, Identity, JoinActiveSessions, K8s, MobileDeviceManagement, OIDC, OktaSCIM,
 	OktaUserSync, Policy, SAML, SessionLocks, UpsellAlert, UsageReporting, LicenseAutoUpdate,
 }
+
+// BackfillFeatures ensures entitlements are backwards compatible.
+// If Entitlements are present, there are no changes.
+// If Entitlements are not present, it sets the entitlements based on legacy field values.
+// TODO(michellescripts) DELETE IN 18.0.0
+func BackfillFeatures(features *proto.Features) {
+	if len(features.Entitlements) > 0 {
+		return
+	}
+
+	features.Entitlements = getBaseEntitlements(features.GetEntitlements())
+
+	// Entitlements: All records are {enabled: false}; update to equal legacy feature value
+	features.Entitlements[string(ExternalAuditStorage)] = &proto.EntitlementInfo{Enabled: features.GetExternalAuditStorage()}
+	features.Entitlements[string(FeatureHiding)] = &proto.EntitlementInfo{Enabled: features.GetFeatureHiding()}
+	features.Entitlements[string(Identity)] = &proto.EntitlementInfo{Enabled: features.GetIdentityGovernance()}
+	features.Entitlements[string(JoinActiveSessions)] = &proto.EntitlementInfo{Enabled: features.GetJoinActiveSessions()}
+	features.Entitlements[string(MobileDeviceManagement)] = &proto.EntitlementInfo{Enabled: features.GetMobileDeviceManagement()}
+	features.Entitlements[string(OIDC)] = &proto.EntitlementInfo{Enabled: features.GetOIDC()}
+	features.Entitlements[string(Policy)] = &proto.EntitlementInfo{Enabled: features.GetPolicy().GetEnabled()}
+	features.Entitlements[string(SAML)] = &proto.EntitlementInfo{Enabled: features.GetSAML()}
+	features.Entitlements[string(K8s)] = &proto.EntitlementInfo{Enabled: features.GetKubernetes()}
+	features.Entitlements[string(App)] = &proto.EntitlementInfo{Enabled: features.GetApp()}
+	features.Entitlements[string(DB)] = &proto.EntitlementInfo{Enabled: features.GetDB()}
+	features.Entitlements[string(Desktop)] = &proto.EntitlementInfo{Enabled: features.GetDesktop()}
+	features.Entitlements[string(HSM)] = &proto.EntitlementInfo{Enabled: features.GetHSM()}
+
+	// set default Identity fields to legacy feature value
+	features.Entitlements[string(AccessLists)] = &proto.EntitlementInfo{Enabled: true, Limit: features.GetAccessList().GetCreateLimit()}
+	features.Entitlements[string(AccessMonitoring)] = &proto.EntitlementInfo{Enabled: features.GetAccessMonitoring().GetEnabled(), Limit: features.GetAccessMonitoring().GetMaxReportRangeLimit()}
+	features.Entitlements[string(AccessRequests)] = &proto.EntitlementInfo{Enabled: features.GetAccessRequests().MonthlyRequestLimit > 0, Limit: features.GetAccessRequests().GetMonthlyRequestLimit()}
+	features.Entitlements[string(DeviceTrust)] = &proto.EntitlementInfo{Enabled: features.GetDeviceTrust().GetEnabled(), Limit: features.GetDeviceTrust().GetDevicesUsageLimit()}
+	// override Identity Package features if Identity is enabled: set true and clear limit
+	if features.GetIdentityGovernance() {
+		features.Entitlements[string(AccessLists)] = &proto.EntitlementInfo{Enabled: true}
+		features.Entitlements[string(AccessMonitoring)] = &proto.EntitlementInfo{Enabled: true}
+		features.Entitlements[string(AccessRequests)] = &proto.EntitlementInfo{Enabled: true}
+		features.Entitlements[string(DeviceTrust)] = &proto.EntitlementInfo{Enabled: true}
+		features.Entitlements[string(OktaSCIM)] = &proto.EntitlementInfo{Enabled: true}
+		features.Entitlements[string(OktaUserSync)] = &proto.EntitlementInfo{Enabled: true}
+		features.Entitlements[string(SessionLocks)] = &proto.EntitlementInfo{Enabled: true}
+	}
+}
+
+// getBaseEntitlements takes a cloud entitlement set and returns a modules Entitlement set
+func getBaseEntitlements(protoEntitlements map[string]*proto.EntitlementInfo) map[string]*proto.EntitlementInfo {
+	all := AllEntitlements
+	result := make(map[string]*proto.EntitlementInfo, len(all))
+
+	for _, e := range all {
+		al, ok := protoEntitlements[string(e)]
+		if !ok {
+			result[string(e)] = &proto.EntitlementInfo{}
+			continue
+		}
+
+		result[string(e)] = &proto.EntitlementInfo{
+			Enabled: al.Enabled,
+			Limit:   al.Limit,
+		}
+	}
+
+	return result
+}
diff --git a/entitlements/entitlements_test.go b/entitlements/entitlements_test.go
new file mode 100644
index 0000000000000..2015f6efaf721
--- /dev/null
+++ b/entitlements/entitlements_test.go
@@ -0,0 +1,286 @@
+// Teleport
+// Copyright (C) 2024 Gravitational, Inc.
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package entitlements
+
+import (
+	"testing"
+
+	"github.com/stretchr/testify/require"
+
+	"github.com/gravitational/teleport/api/client/proto"
+	apiutils "github.com/gravitational/teleport/api/utils"
+)
+
+func TestBackfillFeatures(t *testing.T) {
+	tests := []struct {
+		name     string
+		features *proto.Features
+		expected map[string]*proto.EntitlementInfo
+	}{
+		{
+			name: "entitlements present; keeps entitlement values",
+			features: &proto.Features{
+				DeviceTrust:                nil,
+				AccessRequests:             nil,
+				AccessList:                 nil,
+				AccessMonitoring:           nil,
+				Policy:                     nil,
+				CustomTheme:                "",
+				ProductType:                0,
+				SupportType:                0,
+				Kubernetes:                 false,
+				App:                        false,
+				DB:                         false,
+				OIDC:                       false,
+				SAML:                       false,
+				AccessControls:             false,
+				AdvancedAccessWorkflows:    false,
+				Cloud:                      false,
+				HSM:                        false,
+				Desktop:                    false,
+				RecoveryCodes:              false,
+				Plugins:                    false,
+				AutomaticUpgrades:          false,
+				IsUsageBased:               false,
+				Assist:                     false,
+				FeatureHiding:              false,
+				IdentityGovernance:         false,
+				AccessGraph:                false,
+				Questionnaire:              false,
+				IsStripeManaged:            false,
+				ExternalAuditStorage:       false,
+				JoinActiveSessions:         false,
+				MobileDeviceManagement:     false,
+				AccessMonitoringConfigured: false,
+				Entitlements: map[string]*proto.EntitlementInfo{
+					string(AccessLists):            {Enabled: true, Limit: 111},
+					string(AccessMonitoring):       {Enabled: true, Limit: 2113},
+					string(AccessRequests):         {Enabled: true, Limit: 39},
+					string(App):                    {Enabled: false},
+					string(CloudAuditLogRetention): {Enabled: true},
+					string(DB):                     {Enabled: true},
+					string(Desktop):                {Enabled: true},
+					string(DeviceTrust):            {Enabled: true, Limit: 103},
+					string(ExternalAuditStorage):   {Enabled: true},
+					string(FeatureHiding):          {Enabled: true},
+					string(HSM):                    {Enabled: true},
+					string(Identity):               {Enabled: true},
+					string(JoinActiveSessions):     {Enabled: true},
+					string(K8s):                    {Enabled: true},
+					string(MobileDeviceManagement): {Enabled: true},
+					string(OIDC):                   {Enabled: true},
+					string(OktaSCIM):               {Enabled: true},
+					string(OktaUserSync):           {Enabled: true},
+					string(Policy):                 {Enabled: true},
+					string(SAML):                   {Enabled: true},
+					string(SessionLocks):           {Enabled: true},
+					string(UpsellAlert):            {Enabled: true},
+					string(UsageReporting):         {Enabled: true},
+					string(LicenseAutoUpdate):      {Enabled: true},
+				},
+			},
+			expected: map[string]*proto.EntitlementInfo{
+				string(AccessLists):            {Enabled: true, Limit: 111},
+				string(AccessMonitoring):       {Enabled: true, Limit: 2113},
+				string(AccessRequests):         {Enabled: true, Limit: 39},
+				string(App):                    {Enabled: false},
+				string(CloudAuditLogRetention): {Enabled: true},
+				string(DB):                     {Enabled: true},
+				string(Desktop):                {Enabled: true},
+				string(DeviceTrust):            {Enabled: true, Limit: 103},
+				string(ExternalAuditStorage):   {Enabled: true},
+				string(FeatureHiding):          {Enabled: true},
+				string(HSM):                    {Enabled: true},
+				string(Identity):               {Enabled: true},
+				string(JoinActiveSessions):     {Enabled: true},
+				string(K8s):                    {Enabled: true},
+				string(MobileDeviceManagement): {Enabled: true},
+				string(OIDC):                   {Enabled: true},
+				string(OktaSCIM):               {Enabled: true},
+				string(OktaUserSync):           {Enabled: true},
+				string(Policy):                 {Enabled: true},
+				string(SAML):                   {Enabled: true},
+				string(SessionLocks):           {Enabled: true},
+				string(UpsellAlert):            {Enabled: true},
+				string(UsageReporting):         {Enabled: true},
+				string(LicenseAutoUpdate):      {Enabled: true},
+			},
+		},
+		{
+			name: "entitlements not present; identity on - sets legacy fields & drops limits",
+			features: &proto.Features{
+				DeviceTrust: &proto.DeviceTrustFeature{
+					Enabled:           true,
+					DevicesUsageLimit: 33,
+				},
+				AccessRequests: &proto.AccessRequestsFeature{
+					MonthlyRequestLimit: 22,
+				},
+				AccessList: &proto.AccessListFeature{
+					CreateLimit: 44,
+				},
+				AccessMonitoring: &proto.AccessMonitoringFeature{
+					Enabled:             true,
+					MaxReportRangeLimit: 55,
+				},
+				Policy: &proto.PolicyFeature{
+					Enabled: true,
+				},
+				CustomTheme:                "",
+				ProductType:                0,
+				SupportType:                0,
+				Kubernetes:                 true,
+				App:                        true,
+				DB:                         true,
+				OIDC:                       true,
+				SAML:                       true,
+				AccessControls:             true,
+				AdvancedAccessWorkflows:    true,
+				Cloud:                      true,
+				HSM:                        true,
+				Desktop:                    true,
+				RecoveryCodes:              true,
+				Plugins:                    true,
+				AutomaticUpgrades:          true,
+				IsUsageBased:               true,
+				Assist:                     true,
+				FeatureHiding:              true,
+				IdentityGovernance:         true,
+				AccessGraph:                true,
+				Questionnaire:              true,
+				IsStripeManaged:            true,
+				ExternalAuditStorage:       true,
+				JoinActiveSessions:         true,
+				MobileDeviceManagement:     true,
+				AccessMonitoringConfigured: true,
+			},
+			expected: map[string]*proto.EntitlementInfo{
+				string(AccessLists):            {Enabled: true},
+				string(AccessMonitoring):       {Enabled: true},
+				string(AccessRequests):         {Enabled: true},
+				string(App):                    {Enabled: true},
+				string(DB):                     {Enabled: true},
+				string(Desktop):                {Enabled: true},
+				string(DeviceTrust):            {Enabled: true},
+				string(ExternalAuditStorage):   {Enabled: true},
+				string(FeatureHiding):          {Enabled: true},
+				string(HSM):                    {Enabled: true},
+				string(Identity):               {Enabled: true},
+				string(JoinActiveSessions):     {Enabled: true},
+				string(K8s):                    {Enabled: true},
+				string(MobileDeviceManagement): {Enabled: true},
+				string(OIDC):                   {Enabled: true},
+				string(OktaSCIM):               {Enabled: true},
+				string(OktaUserSync):           {Enabled: true},
+				string(Policy):                 {Enabled: true},
+				string(SAML):                   {Enabled: true},
+				string(SessionLocks):           {Enabled: true},
+				// defaults, no legacy equivalent
+				string(UsageReporting):         {Enabled: false},
+				string(UpsellAlert):            {Enabled: false},
+				string(CloudAuditLogRetention): {Enabled: false},
+				string(LicenseAutoUpdate):      {Enabled: false},
+			},
+		},
+		{
+			name: "entitlements not present; identity off - sets legacy fields",
+			features: &proto.Features{
+				DeviceTrust: &proto.DeviceTrustFeature{
+					Enabled:           true,
+					DevicesUsageLimit: 33,
+				},
+				AccessRequests: &proto.AccessRequestsFeature{
+					MonthlyRequestLimit: 22,
+				},
+				AccessList: &proto.AccessListFeature{
+					CreateLimit: 44,
+				},
+				AccessMonitoring: &proto.AccessMonitoringFeature{
+					Enabled:             true,
+					MaxReportRangeLimit: 55,
+				},
+				Policy: &proto.PolicyFeature{
+					Enabled: true,
+				},
+				CustomTheme:                "",
+				ProductType:                0,
+				SupportType:                0,
+				Kubernetes:                 true,
+				App:                        true,
+				DB:                         true,
+				OIDC:                       true,
+				SAML:                       true,
+				AccessControls:             true,
+				AdvancedAccessWorkflows:    true,
+				Cloud:                      true,
+				HSM:                        true,
+				Desktop:                    true,
+				RecoveryCodes:              true,
+				Plugins:                    true,
+				AutomaticUpgrades:          true,
+				IsUsageBased:               true,
+				Assist:                     true,
+				FeatureHiding:              true,
+				IdentityGovernance:         false,
+				AccessGraph:                true,
+				Questionnaire:              true,
+				IsStripeManaged:            true,
+				ExternalAuditStorage:       true,
+				JoinActiveSessions:         true,
+				MobileDeviceManagement:     true,
+				AccessMonitoringConfigured: true,
+			},
+			expected: map[string]*proto.EntitlementInfo{
+				string(AccessLists):            {Enabled: true, Limit: 44},
+				string(AccessMonitoring):       {Enabled: true, Limit: 55},
+				string(AccessRequests):         {Enabled: true, Limit: 22},
+				string(DeviceTrust):            {Enabled: true, Limit: 33},
+				string(App):                    {Enabled: true},
+				string(DB):                     {Enabled: true},
+				string(Desktop):                {Enabled: true},
+				string(ExternalAuditStorage):   {Enabled: true},
+				string(FeatureHiding):          {Enabled: true},
+				string(HSM):                    {Enabled: true},
+				string(JoinActiveSessions):     {Enabled: true},
+				string(K8s):                    {Enabled: true},
+				string(MobileDeviceManagement): {Enabled: true},
+				string(OIDC):                   {Enabled: true},
+				string(Policy):                 {Enabled: true},
+				string(SAML):                   {Enabled: true},
+
+				// defaults, no legacy equivalent
+				string(UsageReporting):         {Enabled: false},
+				string(UpsellAlert):            {Enabled: false},
+				string(CloudAuditLogRetention): {Enabled: false},
+				string(LicenseAutoUpdate):      {Enabled: false},
+				// Identity off, fields false
+				string(Identity):     {Enabled: false},
+				string(SessionLocks): {Enabled: false},
+				string(OktaSCIM):     {Enabled: false},
+				string(OktaUserSync): {Enabled: false},
+			},
+		},
+	}
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			cloned := apiutils.CloneProtoMsg(tt.features)
+
+			BackfillFeatures(cloned)
+			require.Equal(t, tt.expected, cloned.Entitlements)
+		})
+	}
+}
diff --git a/lib/service/connect.go b/lib/service/connect.go
index 453e241b31a44..40644a73763ee 100644
--- a/lib/service/connect.go
+++ b/lib/service/connect.go
@@ -1087,7 +1087,7 @@ func (process *TeleportProcess) getConnector(clientIdentity, serverIdentity *sta
 	// Set cluster features and return successfully with a working connector.
 	// TODO(michellescripts) remove clone & compatibility check in v18
 	cloned := apiutils.CloneProtoMsg(pingResponse.GetServerFeatures())
-	supportEntitlementsCompatibility(cloned)
+	entitlements.BackfillFeatures(cloned)
 	process.setClusterFeatures(cloned)
 	process.setAuthSubjectiveAddr(pingResponse.RemoteAddr)
 	process.logger.InfoContext(process.ExitContext(), "features loaded from auth server", "identity", clientIdentity.ID.Role, "features", pingResponse.GetServerFeatures())
@@ -1096,70 +1096,6 @@ func (process *TeleportProcess) getConnector(clientIdentity, serverIdentity *sta
 	return newConn, nil
 }
 
-// supportEntitlementsCompatibility ensures entitlements are backwards compatible
-// If Entitlements are present, there are no changes
-// If Entitlements are not present, sets the entitlements fields to legacy field values
-// TODO(michellescripts) remove in v18
-func supportEntitlementsCompatibility(features *proto.Features) {
-	if len(features.Entitlements) > 0 {
-		return
-	}
-
-	features.Entitlements = getBaseEntitlements(features.GetEntitlements())
-
-	// Entitlements: All records are {enabled: false}; update to equal legacy feature value
-	features.Entitlements[string(entitlements.ExternalAuditStorage)] = &proto.EntitlementInfo{Enabled: features.GetExternalAuditStorage()}
-	features.Entitlements[string(entitlements.FeatureHiding)] = &proto.EntitlementInfo{Enabled: features.GetFeatureHiding()}
-	features.Entitlements[string(entitlements.Identity)] = &proto.EntitlementInfo{Enabled: features.GetIdentityGovernance()}
-	features.Entitlements[string(entitlements.JoinActiveSessions)] = &proto.EntitlementInfo{Enabled: features.GetJoinActiveSessions()}
-	features.Entitlements[string(entitlements.MobileDeviceManagement)] = &proto.EntitlementInfo{Enabled: features.GetMobileDeviceManagement()}
-	features.Entitlements[string(entitlements.OIDC)] = &proto.EntitlementInfo{Enabled: features.GetOIDC()}
-	features.Entitlements[string(entitlements.Policy)] = &proto.EntitlementInfo{Enabled: features.GetPolicy().GetEnabled()}
-	features.Entitlements[string(entitlements.SAML)] = &proto.EntitlementInfo{Enabled: features.GetSAML()}
-	features.Entitlements[string(entitlements.K8s)] = &proto.EntitlementInfo{Enabled: features.GetKubernetes()}
-	features.Entitlements[string(entitlements.App)] = &proto.EntitlementInfo{Enabled: features.GetApp()}
-	features.Entitlements[string(entitlements.DB)] = &proto.EntitlementInfo{Enabled: features.GetDB()}
-	features.Entitlements[string(entitlements.Desktop)] = &proto.EntitlementInfo{Enabled: features.GetDesktop()}
-	features.Entitlements[string(entitlements.HSM)] = &proto.EntitlementInfo{Enabled: features.GetHSM()}
-
-	// set default Identity fields to legacy feature value
-	features.Entitlements[string(entitlements.AccessLists)] = &proto.EntitlementInfo{Enabled: true, Limit: features.GetAccessList().GetCreateLimit()}
-	features.Entitlements[string(entitlements.AccessMonitoring)] = &proto.EntitlementInfo{Enabled: features.GetAccessMonitoring().GetEnabled(), Limit: features.GetAccessMonitoring().GetMaxReportRangeLimit()}
-	features.Entitlements[string(entitlements.AccessRequests)] = &proto.EntitlementInfo{Enabled: features.GetAccessRequests().MonthlyRequestLimit > 0, Limit: features.GetAccessRequests().GetMonthlyRequestLimit()}
-	features.Entitlements[string(entitlements.DeviceTrust)] = &proto.EntitlementInfo{Enabled: features.GetDeviceTrust().GetEnabled(), Limit: features.GetDeviceTrust().GetDevicesUsageLimit()}
-	// override Identity Package features if Identity is enabled: set true and clear limit
-	if features.GetIdentityGovernance() {
-		features.Entitlements[string(entitlements.AccessLists)] = &proto.EntitlementInfo{Enabled: true}
-		features.Entitlements[string(entitlements.AccessMonitoring)] = &proto.EntitlementInfo{Enabled: true}
-		features.Entitlements[string(entitlements.AccessRequests)] = &proto.EntitlementInfo{Enabled: true}
-		features.Entitlements[string(entitlements.DeviceTrust)] = &proto.EntitlementInfo{Enabled: true}
-		features.Entitlements[string(entitlements.OktaSCIM)] = &proto.EntitlementInfo{Enabled: true}
-		features.Entitlements[string(entitlements.OktaUserSync)] = &proto.EntitlementInfo{Enabled: true}
-		features.Entitlements[string(entitlements.SessionLocks)] = &proto.EntitlementInfo{Enabled: true}
-	}
-}
-
-// getBaseEntitlements takes a cloud entitlement set and returns a modules Entitlement set
-func getBaseEntitlements(protoEntitlements map[string]*proto.EntitlementInfo) map[string]*proto.EntitlementInfo {
-	all := entitlements.AllEntitlements
-	result := make(map[string]*proto.EntitlementInfo, len(all))
-
-	for _, e := range all {
-		al, ok := protoEntitlements[string(e)]
-		if !ok {
-			result[string(e)] = &proto.EntitlementInfo{}
-			continue
-		}
-
-		result[string(e)] = &proto.EntitlementInfo{
-			Enabled: al.Enabled,
-			Limit:   al.Limit,
-		}
-	}
-
-	return result
-}
-
 // newClient attempts to connect to either the proxy server or auth server
 // For config v3 and onwards, it will only connect to either the proxy (via tunnel) or the auth server (direct),
 // depending on what was specified in the config.
diff --git a/lib/service/connect_test.go b/lib/service/connect_test.go
deleted file mode 100644
index 72f74d4028252..0000000000000
--- a/lib/service/connect_test.go
+++ /dev/null
@@ -1,288 +0,0 @@
-// Teleport
-// Copyright (C) 2024 Gravitational, Inc.
-//
-// This program is free software: you can redistribute it and/or modify
-// it under the terms of the GNU Affero General Public License as published by
-// the Free Software Foundation, either version 3 of the License, or
-// (at your option) any later version.
-//
-// This program is distributed in the hope that it will be useful,
-// but WITHOUT ANY WARRANTY; without even the implied warranty of
-// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
-// GNU Affero General Public License for more details.
-//
-// You should have received a copy of the GNU Affero General Public License
-// along with this program.  If not, see <http://www.gnu.org/licenses/>.
-
-package service
-
-import (
-	"testing"
-
-	"github.com/stretchr/testify/require"
-
-	"github.com/gravitational/teleport/api/client/proto"
-	apiutils "github.com/gravitational/teleport/api/utils"
-	"github.com/gravitational/teleport/entitlements"
-)
-
-func Test_supportEntitlementsCompatibility(t *testing.T) {
-	tests := []struct {
-		name     string
-		features *proto.Features
-		expected map[string]*proto.EntitlementInfo
-	}{
-		{
-			name: "entitlements present; keeps entitlement values",
-			features: &proto.Features{
-				DeviceTrust:                nil,
-				AccessRequests:             nil,
-				AccessList:                 nil,
-				AccessMonitoring:           nil,
-				Policy:                     nil,
-				CustomTheme:                "",
-				ProductType:                0,
-				SupportType:                0,
-				Kubernetes:                 false,
-				App:                        false,
-				DB:                         false,
-				OIDC:                       false,
-				SAML:                       false,
-				AccessControls:             false,
-				AdvancedAccessWorkflows:    false,
-				Cloud:                      false,
-				HSM:                        false,
-				Desktop:                    false,
-				RecoveryCodes:              false,
-				Plugins:                    false,
-				AutomaticUpgrades:          false,
-				IsUsageBased:               false,
-				Assist:                     false,
-				FeatureHiding:              false,
-				IdentityGovernance:         false,
-				AccessGraph:                false,
-				Questionnaire:              false,
-				IsStripeManaged:            false,
-				ExternalAuditStorage:       false,
-				JoinActiveSessions:         false,
-				MobileDeviceManagement:     false,
-				AccessMonitoringConfigured: false,
-				Entitlements: map[string]*proto.EntitlementInfo{
-					string(entitlements.AccessLists):            {Enabled: true, Limit: 111},
-					string(entitlements.AccessMonitoring):       {Enabled: true, Limit: 2113},
-					string(entitlements.AccessRequests):         {Enabled: true, Limit: 39},
-					string(entitlements.App):                    {Enabled: false},
-					string(entitlements.CloudAuditLogRetention): {Enabled: true},
-					string(entitlements.DB):                     {Enabled: true},
-					string(entitlements.Desktop):                {Enabled: true},
-					string(entitlements.DeviceTrust):            {Enabled: true, Limit: 103},
-					string(entitlements.ExternalAuditStorage):   {Enabled: true},
-					string(entitlements.FeatureHiding):          {Enabled: true},
-					string(entitlements.HSM):                    {Enabled: true},
-					string(entitlements.Identity):               {Enabled: true},
-					string(entitlements.JoinActiveSessions):     {Enabled: true},
-					string(entitlements.K8s):                    {Enabled: true},
-					string(entitlements.MobileDeviceManagement): {Enabled: true},
-					string(entitlements.OIDC):                   {Enabled: true},
-					string(entitlements.OktaSCIM):               {Enabled: true},
-					string(entitlements.OktaUserSync):           {Enabled: true},
-					string(entitlements.Policy):                 {Enabled: true},
-					string(entitlements.SAML):                   {Enabled: true},
-					string(entitlements.SessionLocks):           {Enabled: true},
-					string(entitlements.UpsellAlert):            {Enabled: true},
-					string(entitlements.UsageReporting):         {Enabled: true},
-					string(entitlements.LicenseAutoUpdate):      {Enabled: true},
-				},
-			},
-			expected: map[string]*proto.EntitlementInfo{
-				string(entitlements.AccessLists):            {Enabled: true, Limit: 111},
-				string(entitlements.AccessMonitoring):       {Enabled: true, Limit: 2113},
-				string(entitlements.AccessRequests):         {Enabled: true, Limit: 39},
-				string(entitlements.App):                    {Enabled: false},
-				string(entitlements.CloudAuditLogRetention): {Enabled: true},
-				string(entitlements.DB):                     {Enabled: true},
-				string(entitlements.Desktop):                {Enabled: true},
-				string(entitlements.DeviceTrust):            {Enabled: true, Limit: 103},
-				string(entitlements.ExternalAuditStorage):   {Enabled: true},
-				string(entitlements.FeatureHiding):          {Enabled: true},
-				string(entitlements.HSM):                    {Enabled: true},
-				string(entitlements.Identity):               {Enabled: true},
-				string(entitlements.JoinActiveSessions):     {Enabled: true},
-				string(entitlements.K8s):                    {Enabled: true},
-				string(entitlements.MobileDeviceManagement): {Enabled: true},
-				string(entitlements.OIDC):                   {Enabled: true},
-				string(entitlements.OktaSCIM):               {Enabled: true},
-				string(entitlements.OktaUserSync):           {Enabled: true},
-				string(entitlements.Policy):                 {Enabled: true},
-				string(entitlements.SAML):                   {Enabled: true},
-				string(entitlements.SessionLocks):           {Enabled: true},
-				string(entitlements.UpsellAlert):            {Enabled: true},
-				string(entitlements.UsageReporting):         {Enabled: true},
-				string(entitlements.LicenseAutoUpdate):      {Enabled: true},
-			},
-		},
-		{
-			name: "entitlements not present; identity on - sets legacy fields & drops limits",
-			features: &proto.Features{
-				DeviceTrust: &proto.DeviceTrustFeature{
-					Enabled:           true,
-					DevicesUsageLimit: 33,
-				},
-				AccessRequests: &proto.AccessRequestsFeature{
-					MonthlyRequestLimit: 22,
-				},
-				AccessList: &proto.AccessListFeature{
-					CreateLimit: 44,
-				},
-				AccessMonitoring: &proto.AccessMonitoringFeature{
-					Enabled:             true,
-					MaxReportRangeLimit: 55,
-				},
-				Policy: &proto.PolicyFeature{
-					Enabled: true,
-				},
-				CustomTheme:                "",
-				ProductType:                0,
-				SupportType:                0,
-				Kubernetes:                 true,
-				App:                        true,
-				DB:                         true,
-				OIDC:                       true,
-				SAML:                       true,
-				AccessControls:             true,
-				AdvancedAccessWorkflows:    true,
-				Cloud:                      true,
-				HSM:                        true,
-				Desktop:                    true,
-				RecoveryCodes:              true,
-				Plugins:                    true,
-				AutomaticUpgrades:          true,
-				IsUsageBased:               true,
-				Assist:                     true,
-				FeatureHiding:              true,
-				IdentityGovernance:         true,
-				AccessGraph:                true,
-				Questionnaire:              true,
-				IsStripeManaged:            true,
-				ExternalAuditStorage:       true,
-				JoinActiveSessions:         true,
-				MobileDeviceManagement:     true,
-				AccessMonitoringConfigured: true,
-			},
-			expected: map[string]*proto.EntitlementInfo{
-				string(entitlements.AccessLists):            {Enabled: true},
-				string(entitlements.AccessMonitoring):       {Enabled: true},
-				string(entitlements.AccessRequests):         {Enabled: true},
-				string(entitlements.App):                    {Enabled: true},
-				string(entitlements.DB):                     {Enabled: true},
-				string(entitlements.Desktop):                {Enabled: true},
-				string(entitlements.DeviceTrust):            {Enabled: true},
-				string(entitlements.ExternalAuditStorage):   {Enabled: true},
-				string(entitlements.FeatureHiding):          {Enabled: true},
-				string(entitlements.HSM):                    {Enabled: true},
-				string(entitlements.Identity):               {Enabled: true},
-				string(entitlements.JoinActiveSessions):     {Enabled: true},
-				string(entitlements.K8s):                    {Enabled: true},
-				string(entitlements.MobileDeviceManagement): {Enabled: true},
-				string(entitlements.OIDC):                   {Enabled: true},
-				string(entitlements.OktaSCIM):               {Enabled: true},
-				string(entitlements.OktaUserSync):           {Enabled: true},
-				string(entitlements.Policy):                 {Enabled: true},
-				string(entitlements.SAML):                   {Enabled: true},
-				string(entitlements.SessionLocks):           {Enabled: true},
-				// defaults, no legacy equivalent
-				string(entitlements.UsageReporting):         {Enabled: false},
-				string(entitlements.UpsellAlert):            {Enabled: false},
-				string(entitlements.CloudAuditLogRetention): {Enabled: false},
-				string(entitlements.LicenseAutoUpdate):      {Enabled: false},
-			},
-		},
-		{
-			name: "entitlements not present; identity off - sets legacy fields",
-			features: &proto.Features{
-				DeviceTrust: &proto.DeviceTrustFeature{
-					Enabled:           true,
-					DevicesUsageLimit: 33,
-				},
-				AccessRequests: &proto.AccessRequestsFeature{
-					MonthlyRequestLimit: 22,
-				},
-				AccessList: &proto.AccessListFeature{
-					CreateLimit: 44,
-				},
-				AccessMonitoring: &proto.AccessMonitoringFeature{
-					Enabled:             true,
-					MaxReportRangeLimit: 55,
-				},
-				Policy: &proto.PolicyFeature{
-					Enabled: true,
-				},
-				CustomTheme:                "",
-				ProductType:                0,
-				SupportType:                0,
-				Kubernetes:                 true,
-				App:                        true,
-				DB:                         true,
-				OIDC:                       true,
-				SAML:                       true,
-				AccessControls:             true,
-				AdvancedAccessWorkflows:    true,
-				Cloud:                      true,
-				HSM:                        true,
-				Desktop:                    true,
-				RecoveryCodes:              true,
-				Plugins:                    true,
-				AutomaticUpgrades:          true,
-				IsUsageBased:               true,
-				Assist:                     true,
-				FeatureHiding:              true,
-				IdentityGovernance:         false,
-				AccessGraph:                true,
-				Questionnaire:              true,
-				IsStripeManaged:            true,
-				ExternalAuditStorage:       true,
-				JoinActiveSessions:         true,
-				MobileDeviceManagement:     true,
-				AccessMonitoringConfigured: true,
-			},
-			expected: map[string]*proto.EntitlementInfo{
-				string(entitlements.AccessLists):            {Enabled: true, Limit: 44},
-				string(entitlements.AccessMonitoring):       {Enabled: true, Limit: 55},
-				string(entitlements.AccessRequests):         {Enabled: true, Limit: 22},
-				string(entitlements.DeviceTrust):            {Enabled: true, Limit: 33},
-				string(entitlements.App):                    {Enabled: true},
-				string(entitlements.DB):                     {Enabled: true},
-				string(entitlements.Desktop):                {Enabled: true},
-				string(entitlements.ExternalAuditStorage):   {Enabled: true},
-				string(entitlements.FeatureHiding):          {Enabled: true},
-				string(entitlements.HSM):                    {Enabled: true},
-				string(entitlements.JoinActiveSessions):     {Enabled: true},
-				string(entitlements.K8s):                    {Enabled: true},
-				string(entitlements.MobileDeviceManagement): {Enabled: true},
-				string(entitlements.OIDC):                   {Enabled: true},
-				string(entitlements.Policy):                 {Enabled: true},
-				string(entitlements.SAML):                   {Enabled: true},
-
-				// defaults, no legacy equivalent
-				string(entitlements.UsageReporting):         {Enabled: false},
-				string(entitlements.UpsellAlert):            {Enabled: false},
-				string(entitlements.CloudAuditLogRetention): {Enabled: false},
-				string(entitlements.LicenseAutoUpdate):      {Enabled: false},
-
-				// Identity off, fields false
-				string(entitlements.Identity):     {Enabled: false},
-				string(entitlements.SessionLocks): {Enabled: false},
-				string(entitlements.OktaSCIM):     {Enabled: false},
-				string(entitlements.OktaUserSync): {Enabled: false},
-			},
-		},
-	}
-	for _, tt := range tests {
-		t.Run(tt.name, func(t *testing.T) {
-			cloned := apiutils.CloneProtoMsg(tt.features)
-
-			supportEntitlementsCompatibility(cloned)
-			require.Equal(t, tt.expected, cloned.Entitlements)
-		})
-	}
-}
diff --git a/lib/service/service.go b/lib/service/service.go
index c36e15e33420b..54ec59037bf15 100644
--- a/lib/service/service.go
+++ b/lib/service/service.go
@@ -4595,6 +4595,7 @@ func (process *TeleportProcess) initProxyEndpoint(conn *Connector) error {
 			TracerProvider:            process.TracingProvider,
 			AutomaticUpgradesChannels: cfg.Proxy.AutomaticUpgradesChannels,
 			IntegrationAppHandler:     connectionsHandler,
+			FeatureWatchInterval:      utils.HalfJitter(web.DefaultFeatureWatchInterval * 2),
 		}
 		webHandler, err := web.NewHandler(webConfig)
 		if err != nil {
diff --git a/lib/web/apiserver.go b/lib/web/apiserver.go
index 0e05fb23c9c2d..921abf023213a 100644
--- a/lib/web/apiserver.go
+++ b/lib/web/apiserver.go
@@ -21,6 +21,7 @@
 package web
 
 import (
+	"cmp"
 	"context"
 	"crypto/tls"
 	"encoding/base64"
@@ -124,6 +125,9 @@ const (
 	IncludedResourceModeRequestable = "requestable"
 	// IncludedResourceModeAll describes that all resources, requestable and available, should be returned.
 	IncludedResourceModeAll = "all"
+	// DefaultFeatureWatchInterval is the default time in which the feature watcher
+	// should ping the auth server to check for updated features
+	DefaultFeatureWatchInterval = time.Minute * 5
 )
 
 // healthCheckAppServerFunc defines a function used to perform a health check
@@ -153,12 +157,8 @@ type Handler struct {
 	// userConns tracks amount of current active connections with user certificates.
 	userConns atomic.Int32
 
-	// ClusterFeatures contain flags for supported and unsupported features.
-	// Note: This field can become stale since it's only set on initial proxy
-	// startup. To get the latest feature flags you'll need to ping from the
-	// auth server.
-	// https://github.com/gravitational/teleport/issues/39161
-	ClusterFeatures proto.Features
+	// clusterFeatures contain flags for supported and unsupported features.
+	clusterFeatures proto.Features
 
 	// nodeWatcher is a services.NodeWatcher used by Assist to lookup nodes from
 	// the proxy's cache and get nodes in real time.
@@ -314,6 +314,10 @@ type Config struct {
 
 	// IntegrationAppHandler handles App Access requests which use an Integration.
 	IntegrationAppHandler app.ServerHandler
+
+	// FeatureWatchInterval is the interval between pings to the auth server
+	// to fetch new cluster features
+	FeatureWatchInterval time.Duration
 }
 
 // SetDefaults ensures proper default values are set if
@@ -328,6 +332,8 @@ func (c *Config) SetDefaults() {
 	if c.PresenceChecker == nil {
 		c.PresenceChecker = client.RunPresenceTask
 	}
+
+	c.FeatureWatchInterval = cmp.Or(c.FeatureWatchInterval, DefaultFeatureWatchInterval)
 }
 
 type APIHandler struct {
@@ -451,7 +457,7 @@ func NewHandler(cfg Config, opts ...HandlerOption) (*APIHandler, error) {
 		log:                  newPackageLogger(),
 		logger:               slog.Default().With(teleport.ComponentKey, teleport.ComponentWeb),
 		clock:                clockwork.NewRealClock(),
-		ClusterFeatures:      cfg.ClusterFeatures,
+		clusterFeatures:      cfg.ClusterFeatures,
 		healthCheckAppServer: cfg.HealthCheckAppServer,
 		tracer:               cfg.TracerProvider.Tracer(teleport.ComponentWeb),
 		wsIODeadline:         wsIODeadline,
@@ -682,6 +688,8 @@ func NewHandler(cfg Config, opts ...HandlerOption) (*APIHandler, error) {
 		}
 	}
 
+	go h.startFeatureWatcher()
+
 	return &APIHandler{
 		handler:    h,
 		appHandler: appHandler,
@@ -1164,17 +1172,12 @@ func (h *Handler) getUserContext(w http.ResponseWriter, r *http.Request, p httpr
 	}
 	desktopRecordingEnabled := recConfig.GetMode() != types.RecordOff
 
-	pingResp, err := clt.Ping(r.Context())
-	if err != nil {
-		return nil, trace.Wrap(err)
-	}
-
-	features := pingResp.GetServerFeatures()
-	entitlement := modules.GetProtoEntitlement(features, entitlements.AccessMonitoring)
+	features := h.GetClusterFeatures()
+	entitlement := modules.GetProtoEntitlement(&features, entitlements.AccessMonitoring)
 	// ensure entitlement is set & feature is configured
 	accessMonitoringEnabled := entitlement.Enabled && features.GetAccessMonitoringConfigured()
 
-	userContext, err := ui.NewUserContext(user, accessChecker.Roles(), *pingResp.ServerFeatures, desktopRecordingEnabled, accessMonitoringEnabled)
+	userContext, err := ui.NewUserContext(user, accessChecker.Roles(), features, desktopRecordingEnabled, accessMonitoringEnabled)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
@@ -1692,14 +1695,7 @@ func (h *Handler) getWebConfig(w http.ResponseWriter, r *http.Request, p httprou
 		}
 	}
 
-	clusterFeatures := h.ClusterFeatures
-	// ping server to get cluster features since h.ClusterFeatures may be stale
-	pingResponse, err := h.GetProxyClient().Ping(r.Context())
-	if err != nil {
-		h.log.WithError(err).Warn("Cannot retrieve cluster features, client may receive stale features")
-	} else {
-		clusterFeatures = *pingResponse.ServerFeatures
-	}
+	clusterFeatures := h.GetClusterFeatures()
 
 	// get tunnel address to display on cloud instances
 	tunnelPublicAddr := ""
@@ -1813,7 +1809,6 @@ func setEntitlementsWithLegacyLogic(webCfg *webclient.WebConfig, clusterFeatures
 		webCfg.Entitlements[string(entitlements.OIDC)] = webclient.EntitlementInfo{Enabled: clusterFeatures.GetOIDC()}
 		webCfg.Entitlements[string(entitlements.Policy)] = webclient.EntitlementInfo{Enabled: clusterFeatures.GetPolicy() != nil && clusterFeatures.GetPolicy().Enabled}
 		webCfg.Entitlements[string(entitlements.SAML)] = webclient.EntitlementInfo{Enabled: clusterFeatures.GetSAML()}
-
 		// set default Identity fields to legacy feature value
 		webCfg.Entitlements[string(entitlements.AccessLists)] = webclient.EntitlementInfo{Enabled: true, Limit: clusterFeatures.GetAccessList().GetCreateLimit()}
 		webCfg.Entitlements[string(entitlements.AccessMonitoring)] = webclient.EntitlementInfo{Enabled: clusterFeatures.GetAccessMonitoring().GetEnabled(), Limit: clusterFeatures.GetAccessMonitoring().GetMaxReportRangeLimit()}
diff --git a/lib/web/apiserver_test.go b/lib/web/apiserver_test.go
index 1719dd66b5a21..640b7395ea7ee 100644
--- a/lib/web/apiserver_test.go
+++ b/lib/web/apiserver_test.go
@@ -4561,6 +4561,7 @@ func TestApplicationWebSessionsDeletedAfterLogout(t *testing.T) {
 func TestGetWebConfig_WithEntitlements(t *testing.T) {
 	ctx := context.Background()
 	env := newWebPack(t, 1)
+	handler := env.proxies[0].handler.handler
 
 	// Set auth preference with passwordless.
 	const MOTD = "Welcome to cluster, your activity will be recorded."
@@ -4591,6 +4592,9 @@ func TestGetWebConfig_WithEntitlements(t *testing.T) {
 	_, err = env.server.Auth().UpsertGithubConnector(ctx, github)
 	require.NoError(t, err)
 
+	// start the feature watcher so the web config gets new features
+	env.clock.Advance(DefaultFeatureWatchInterval * 2)
+
 	expectedCfg := webclient.WebConfig{
 		Auth: webclient.WebConfigAuthSettings{
 			SecondFactor: constants.SecondFactorOptional,
@@ -4680,6 +4684,7 @@ func TestGetWebConfig_WithEntitlements(t *testing.T) {
 			},
 		},
 	})
+	env.clock.Advance(DefaultFeatureWatchInterval * 2)
 
 	require.NoError(t, err)
 	// This version is too high and MUST NOT be used
@@ -4690,7 +4695,7 @@ func TestGetWebConfig_WithEntitlements(t *testing.T) {
 		},
 	}
 	require.NoError(t, channels.CheckAndSetDefaults())
-	env.proxies[0].handler.handler.cfg.AutomaticUpgradesChannels = channels
+	handler.cfg.AutomaticUpgradesChannels = channels
 
 	expectedCfg.IsCloud = true
 	expectedCfg.IsUsageBasedBilling = true
@@ -4706,14 +4711,20 @@ func TestGetWebConfig_WithEntitlements(t *testing.T) {
 	expectedCfg.Entitlements[string(entitlements.JoinActiveSessions)] = webclient.EntitlementInfo{Enabled: false}
 	expectedCfg.Entitlements[string(entitlements.K8s)] = webclient.EntitlementInfo{Enabled: false}
 
-	// request and verify enabled features are enabled.
-	re, err = clt.Get(ctx, endpoint, nil)
-	require.NoError(t, err)
-	require.True(t, strings.HasPrefix(string(re.Bytes()), "var GRV_CONFIG"))
-	str = strings.ReplaceAll(string(re.Bytes()), "var GRV_CONFIG = ", "")
-	err = json.Unmarshal([]byte(str[:len(str)-1]), &cfg)
-	require.NoError(t, err)
-	require.Equal(t, expectedCfg, cfg)
+	// request and verify enabled features are eventually enabled.
+	require.EventuallyWithT(t, func(t *assert.CollectT) {
+		re, err := clt.Get(ctx, endpoint, nil)
+		if !assert.NoError(t, err) {
+			return
+		}
+		assert.True(t, bytes.HasPrefix(re.Bytes(), []byte("var GRV_CONFIG")))
+		res := bytes.ReplaceAll(re.Bytes(), []byte("var GRV_CONFIG = "), []byte{})
+		err = json.Unmarshal(res[:len(res)-1], &cfg)
+		assert.NoError(t, err)
+		diff := cmp.Diff(expectedCfg, cfg)
+		assert.Empty(t, diff)
+
+	}, time.Second*5, time.Millisecond*50)
 
 	// use mock client to assert that if ping returns an error, we'll default to
 	// cluster config
@@ -4736,15 +4747,22 @@ func TestGetWebConfig_WithEntitlements(t *testing.T) {
 			IsUsageBasedBilling: false,
 		},
 	})
+	env.clock.Advance(DefaultFeatureWatchInterval * 2)
 
 	// request and verify again
-	re, err = clt.Get(ctx, endpoint, nil)
-	require.NoError(t, err)
-	require.True(t, strings.HasPrefix(string(re.Bytes()), "var GRV_CONFIG"))
-	str = strings.ReplaceAll(string(re.Bytes()), "var GRV_CONFIG = ", "")
-	err = json.Unmarshal([]byte(str[:len(str)-1]), &cfg)
-	require.NoError(t, err)
-	require.Equal(t, expectedCfg, cfg)
+	require.EventuallyWithT(t, func(t *assert.CollectT) {
+		re, err := clt.Get(ctx, endpoint, nil)
+		if !assert.NoError(t, err) {
+			return
+		}
+		assert.True(t, bytes.HasPrefix(re.Bytes(), []byte("var GRV_CONFIG")))
+		res := bytes.ReplaceAll(re.Bytes(), []byte("var GRV_CONFIG = "), []byte{})
+		err = json.Unmarshal(res[:len(res)-1], &cfg)
+		assert.NoError(t, err)
+		diff := cmp.Diff(expectedCfg, cfg)
+		assert.Empty(t, diff)
+
+	}, time.Second*5, time.Millisecond*50)
 }
 
 func TestGetWebConfig_LegacyFeatureLimits(t *testing.T) {
@@ -4764,6 +4782,8 @@ func TestGetWebConfig_LegacyFeatureLimits(t *testing.T) {
 			},
 		},
 	})
+	// start the feature watcher so the web config gets new features
+	env.clock.Advance(DefaultFeatureWatchInterval * 2)
 
 	expectedCfg := webclient.WebConfig{
 		Auth: webclient.WebConfigAuthSettings{
@@ -4812,20 +4832,25 @@ func TestGetWebConfig_LegacyFeatureLimits(t *testing.T) {
 		PlayableDatabaseProtocols: player.SupportedDatabaseProtocols,
 	}
 
-	// Make a request.
 	clt := env.proxies[0].newClient(t)
-	endpoint := clt.Endpoint("web", "config.js")
-	re, err := clt.Get(ctx, endpoint, nil)
-	require.NoError(t, err)
-	require.True(t, strings.HasPrefix(string(re.Bytes()), "var GRV_CONFIG"))
-
-	// Response is type application/javascript, we need to strip off the variable name
-	// and the semicolon at the end, then we are left with json like object.
-	var cfg webclient.WebConfig
-	str := strings.ReplaceAll(string(re.Bytes()), "var GRV_CONFIG = ", "")
-	err = json.Unmarshal([]byte(str[:len(str)-1]), &cfg)
-	require.NoError(t, err)
-	require.Equal(t, expectedCfg, cfg)
+	require.EventuallyWithT(t, func(t *assert.CollectT) {
+		// Make a request.
+		endpoint := clt.Endpoint("web", "config.js")
+		re, err := clt.Get(ctx, endpoint, nil)
+		if !assert.NoError(t, err) {
+			return
+		}
+		assert.True(t, bytes.HasPrefix(re.Bytes(), []byte("var GRV_CONFIG")))
+
+		// Response is type application/javascript, we need to strip off the variable name
+		// and the semicolon at the end, then we are left with json like object.
+		var cfg webclient.WebConfig
+		res := bytes.ReplaceAll(re.Bytes(), []byte("var GRV_CONFIG = "), []byte{})
+		err = json.Unmarshal(res[:len(res)-1], &cfg)
+		assert.NoError(t, err)
+		diff := cmp.Diff(expectedCfg, cfg)
+		assert.Empty(t, diff)
+	}, time.Second*5, time.Millisecond*50)
 }
 
 func TestCreatePrivilegeToken(t *testing.T) {
diff --git a/lib/web/features.go b/lib/web/features.go
new file mode 100644
index 0000000000000..29798851aa7ce
--- /dev/null
+++ b/lib/web/features.go
@@ -0,0 +1,73 @@
+/*
+ * Teleport
+ * Copyright (C) 2024  Gravitational, Inc.
+ *
+ * This program is free software: you can redistribute it and/or modify
+ * it under the terms of the GNU Affero General Public License as published by
+ * the Free Software Foundation, either version 3 of the License, or
+ * (at your option) any later version.
+ *
+ * This program is distributed in the hope that it will be useful,
+ * but WITHOUT ANY WARRANTY; without even the implied warranty of
+ * MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+ * GNU Affero General Public License for more details.
+ *
+ * You should have received a copy of the GNU Affero General Public License
+ * along with this program.  If not, see <http://www.gnu.org/licenses/>.
+ */
+
+package web
+
+import (
+	"github.com/gravitational/teleport/api/client/proto"
+	"github.com/gravitational/teleport/entitlements"
+)
+
+// SetClusterFeatures sets the flags for supported and unsupported features.
+// TODO(mcbattirola): make method unexported, fix tests using it to set
+// test modules instead.
+func (h *Handler) SetClusterFeatures(features proto.Features) {
+	h.Mutex.Lock()
+	defer h.Mutex.Unlock()
+
+	entitlements.BackfillFeatures(&features)
+	h.clusterFeatures = features
+}
+
+// GetClusterFeatures returns flags for supported and unsupported features.
+func (h *Handler) GetClusterFeatures() proto.Features {
+	h.Mutex.Lock()
+	defer h.Mutex.Unlock()
+
+	return h.clusterFeatures
+}
+
+// startFeatureWatcher periodically pings the auth server and updates `clusterFeatures`.
+// Must be called only once per `handler`, otherwise it may close an already closed channel
+// which will cause a panic.
+// The watcher doesn't ping the auth server immediately upon start because features are
+// already set by the config object in `NewHandler`.
+func (h *Handler) startFeatureWatcher() {
+	ticker := h.clock.NewTicker(h.cfg.FeatureWatchInterval)
+	h.log.WithField("interval", h.cfg.FeatureWatchInterval).Info("Proxy handler features watcher has started")
+	ctx := h.cfg.Context
+
+	defer ticker.Stop()
+	for {
+		select {
+		case <-ticker.Chan():
+			h.log.Info("Pinging auth server for features")
+			pingResponse, err := h.GetProxyClient().Ping(ctx)
+			if err != nil {
+				h.log.WithError(err).Error("Auth server ping failed")
+				continue
+			}
+
+			h.SetClusterFeatures(*pingResponse.ServerFeatures)
+			h.log.WithField("features", pingResponse.ServerFeatures).Info("Done updating proxy features")
+		case <-ctx.Done():
+			h.log.Info("Feature service has stopped")
+			return
+		}
+	}
+}
diff --git a/lib/web/features_test.go b/lib/web/features_test.go
new file mode 100644
index 0000000000000..3798e819b46eb
--- /dev/null
+++ b/lib/web/features_test.go
@@ -0,0 +1,176 @@
+/*
+ * Teleport
+ * Copyright (C) 2024  Gravitational, Inc.
+ *
+ * This program is free software: you can redistribute it and/or modify
+ * it under the terms of the GNU Affero General Public License as published by
+ * the Free Software Foundation, either version 3 of the License, or
+ * (at your option) any later version.
+ *
+ * This program is distributed in the hope that it will be useful,
+ * but WITHOUT ANY WARRANTY; without even the implied warranty of
+ * MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+ * GNU Affero General Public License for more details.
+ *
+ * You should have received a copy of the GNU Affero General Public License
+ * along with this program.  If not, see <http://www.gnu.org/licenses/>.
+ */
+
+package web
+
+import (
+	"context"
+	"log/slog"
+	"testing"
+	"time"
+
+	"github.com/google/go-cmp/cmp"
+	"github.com/jonboulle/clockwork"
+	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+
+	"github.com/gravitational/teleport"
+	"github.com/gravitational/teleport/api/client/proto"
+	"github.com/gravitational/teleport/api/utils"
+	"github.com/gravitational/teleport/entitlements"
+	"github.com/gravitational/teleport/lib/auth/authclient"
+)
+
+// mockedPingTestProxy is a test proxy with a mocked Ping method
+// that returns the internal features
+type mockedFeatureGetter struct {
+	authclient.ClientI
+	features proto.Features
+}
+
+func (m *mockedFeatureGetter) Ping(ctx context.Context) (proto.PingResponse, error) {
+	return proto.PingResponse{
+		ServerFeatures: utils.CloneProtoMsg(&m.features),
+	}, nil
+}
+
+func (m *mockedFeatureGetter) setFeatures(f proto.Features) {
+	m.features = f
+}
+
+func TestFeaturesWatcher(t *testing.T) {
+	clock := clockwork.NewFakeClock()
+
+	mockClient := &mockedFeatureGetter{features: proto.Features{
+		Kubernetes:     true,
+		Entitlements:   map[string]*proto.EntitlementInfo{},
+		AccessRequests: &proto.AccessRequestsFeature{},
+	}}
+
+	ctx, cancel := context.WithCancel(context.Background())
+	handler := &Handler{
+		cfg: Config{
+			FeatureWatchInterval: 100 * time.Millisecond,
+			ProxyClient:          mockClient,
+			Context:              ctx,
+		},
+		clock:           clock,
+		clusterFeatures: proto.Features{},
+		log:             newPackageLogger(),
+		logger:          slog.Default().With(teleport.ComponentKey, teleport.ComponentWeb),
+	}
+
+	// before running the watcher, features should match the value passed to the handler
+	requireFeatures(t, clock, proto.Features{}, handler.GetClusterFeatures)
+
+	go handler.startFeatureWatcher()
+	clock.BlockUntil(1)
+
+	// after starting the watcher, handler.GetClusterFeatures should return
+	// values matching the client's response
+	features := proto.Features{
+		Kubernetes:     true,
+		Entitlements:   map[string]*proto.EntitlementInfo{},
+		AccessRequests: &proto.AccessRequestsFeature{},
+	}
+	entitlements.BackfillFeatures(&features)
+	expected := utils.CloneProtoMsg(&features)
+	requireFeatures(t, clock, *expected, handler.GetClusterFeatures)
+
+	// update values once again and check if the features are properly updated
+	features = proto.Features{
+		Kubernetes:     false,
+		Entitlements:   map[string]*proto.EntitlementInfo{},
+		AccessRequests: &proto.AccessRequestsFeature{},
+	}
+	entitlements.BackfillFeatures(&features)
+	mockClient.setFeatures(features)
+	expected = utils.CloneProtoMsg(&features)
+	requireFeatures(t, clock, *expected, handler.GetClusterFeatures)
+
+	// test updating entitlements
+	features = proto.Features{
+		Kubernetes: true,
+		Entitlements: map[string]*proto.EntitlementInfo{
+			string(entitlements.ExternalAuditStorage):   {Enabled: true},
+			string(entitlements.AccessLists):            {Enabled: true},
+			string(entitlements.AccessMonitoring):       {Enabled: true},
+			string(entitlements.App):                    {Enabled: true},
+			string(entitlements.CloudAuditLogRetention): {Enabled: true},
+		},
+		AccessRequests: &proto.AccessRequestsFeature{},
+	}
+	entitlements.BackfillFeatures(&features)
+	mockClient.setFeatures(features)
+
+	expected = &proto.Features{
+		Kubernetes: true,
+		Entitlements: map[string]*proto.EntitlementInfo{
+			string(entitlements.ExternalAuditStorage):   {Enabled: true},
+			string(entitlements.AccessLists):            {Enabled: true},
+			string(entitlements.AccessMonitoring):       {Enabled: true},
+			string(entitlements.App):                    {Enabled: true},
+			string(entitlements.CloudAuditLogRetention): {Enabled: true},
+		},
+		AccessRequests: &proto.AccessRequestsFeature{},
+	}
+	entitlements.BackfillFeatures(expected)
+	requireFeatures(t, clock, *expected, handler.GetClusterFeatures)
+
+	// stop watcher and ensure it stops updating features
+	cancel()
+	features = proto.Features{
+		Kubernetes:     !features.Kubernetes,
+		App:            !features.App,
+		DB:             true,
+		Entitlements:   map[string]*proto.EntitlementInfo{},
+		AccessRequests: &proto.AccessRequestsFeature{},
+	}
+	entitlements.BackfillFeatures(&features)
+	mockClient.setFeatures(features)
+	notExpected := utils.CloneProtoMsg(&features)
+	// assert the handler never get these last features as the watcher is stopped
+	neverFeatures(t, clock, *notExpected, handler.GetClusterFeatures)
+}
+
+// requireFeatures is a helper function that advances the clock, then
+// calls `getFeatures` every 100ms for up to 1 second, until it
+// returns the expected result (`want`).
+func requireFeatures(t *testing.T, fakeClock clockwork.FakeClock, want proto.Features, getFeatures func() proto.Features) {
+	t.Helper()
+
+	// Advance the clock so the service fetch and stores features
+	fakeClock.Advance(1 * time.Second)
+
+	require.EventuallyWithT(t, func(t *assert.CollectT) {
+		diff := cmp.Diff(want, getFeatures())
+		assert.Empty(t, diff)
+	}, 5*time.Second, time.Millisecond*100)
+}
+
+// neverFeatures is a helper function that advances the clock, then
+// calls `getFeatures` every 100ms for up to 1 second. If at some point `getFeatures`
+// returns `doNotWant`, the test fails.
+func neverFeatures(t *testing.T, fakeClock clockwork.FakeClock, doNotWant proto.Features, getFeatures func() proto.Features) {
+	t.Helper()
+
+	fakeClock.Advance(1 * time.Second)
+	require.Never(t, func() bool {
+		return cmp.Diff(doNotWant, getFeatures()) == ""
+	}, 1*time.Second, time.Millisecond*100)
+}
diff --git a/lib/web/integrations_awsoidc.go b/lib/web/integrations_awsoidc.go
index 6252af38a3d72..2ab0a00492d89 100644
--- a/lib/web/integrations_awsoidc.go
+++ b/lib/web/integrations_awsoidc.go
@@ -148,7 +148,7 @@ func (h *Handler) awsOIDCDeployService(w http.ResponseWriter, r *http.Request, p
 	}
 
 	teleportVersionTag := teleport.Version
-	if automaticUpgrades(h.ClusterFeatures) {
+	if automaticUpgrades(h.GetClusterFeatures()) {
 		cloudStableVersion, err := h.cfg.AutomaticUpgradesChannels.DefaultVersion(ctx)
 		if err != nil {
 			return "", trace.Wrap(err)
@@ -201,7 +201,7 @@ func (h *Handler) awsOIDCDeployDatabaseServices(w http.ResponseWriter, r *http.R
 	}
 
 	teleportVersionTag := teleport.Version
-	if automaticUpgrades(h.ClusterFeatures) {
+	if automaticUpgrades(h.GetClusterFeatures()) {
 		cloudStableVersion, err := h.cfg.AutomaticUpgradesChannels.DefaultVersion(ctx)
 		if err != nil {
 			return "", trace.Wrap(err)
@@ -527,7 +527,7 @@ func (h *Handler) awsOIDCEnrollEKSClusters(w http.ResponseWriter, r *http.Reques
 		return nil, trace.BadParameter("an integration name is required")
 	}
 
-	agentVersion, err := kubeutils.GetKubeAgentVersion(ctx, h.cfg.ProxyClient, h.ClusterFeatures, h.cfg.AutomaticUpgradesChannels)
+	agentVersion, err := kubeutils.GetKubeAgentVersion(ctx, h.cfg.ProxyClient, h.GetClusterFeatures(), h.cfg.AutomaticUpgradesChannels)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
diff --git a/lib/web/join_tokens.go b/lib/web/join_tokens.go
index c5939e30953d7..7dcd657857ab4 100644
--- a/lib/web/join_tokens.go
+++ b/lib/web/join_tokens.go
@@ -377,7 +377,7 @@ func (h *Handler) createTokenForDiscoveryHandle(w http.ResponseWriter, r *http.R
 func (h *Handler) getAutoUpgrades(ctx context.Context) (bool, string, error) {
 	var autoUpgradesVersion string
 	var err error
-	autoUpgrades := automaticUpgrades(h.ClusterFeatures)
+	autoUpgrades := automaticUpgrades(h.GetClusterFeatures())
 	if autoUpgrades {
 		autoUpgradesVersion, err = h.cfg.AutomaticUpgradesChannels.DefaultVersion(ctx)
 		if err != nil {