diff --git a/Cargo.lock b/Cargo.lock
index 69b752d4f83c1..68e9a40c1c6ba 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -13213,7 +13213,7 @@ checksum = "accd4ea62f7bb7a82fe23066fb0957d48ef677f6eeb8215f372f52e48bb32426"
 
 [[package]]
 name = "vdev"
-version = "0.3.35"
+version = "0.3.36"
 dependencies = [
  "anyhow",
  "cfg-if",
diff --git a/Makefile b/Makefile
index 4ba5895cc7c80..baa6aafab5c11 100644
--- a/Makefile
+++ b/Makefile
@@ -304,9 +304,6 @@ test-integration-%-cleanup:
 
 test-integration-%:
 	$(VDEV) --verbose integration test $*
-ifeq ($(AUTODESPAWN), true)
-	make test-integration-$*-cleanup
-endif
 
 .PHONY: test-e2e-kubernetes
 test-e2e-kubernetes: ## Runs Kubernetes E2E tests
diff --git a/vdev/Cargo.toml b/vdev/Cargo.toml
index e314d17c7067f..f4eb71c9d25fc 100644
--- a/vdev/Cargo.toml
+++ b/vdev/Cargo.toml
@@ -1,6 +1,6 @@
 [package]
 name = "vdev"
-version = "0.3.35"
+version = "0.3.36"
 edition = "2024"
 authors = ["Vector Contributors <vector@datadoghq.com>"]
 license = "MPL-2.0"
diff --git a/vdev/src/commands/compose_tests/test.rs b/vdev/src/commands/compose_tests/test.rs
index b8bcbcb0c7d02..7898a8fcd7680 100644
--- a/vdev/src/commands/compose_tests/test.rs
+++ b/vdev/src/commands/compose_tests/test.rs
@@ -10,6 +10,52 @@ use crate::testing::{
 
 use super::active_projects::find_active_environment_for_integration;
 
+/// RAII guard that triggers test environment cleanup.
+///
+/// Cleanup is skipped if disabled via `AUTODESPAWN` or `AUTOSPAWN` environment
+/// variables, or if the environment was already running prior to the test execution
+/// (preserving caller-owned environments and fast repeated runs).
+struct DespawnGuard<'a> {
+    local_config: ComposeTestLocalConfig,
+    test_name: &'a str,
+    should_despawn: bool,
+}
+
+impl<'a> DespawnGuard<'a> {
+    pub fn new(
+        local_config: ComposeTestLocalConfig,
+        test_name: &'a str,
+        was_running: bool,
+    ) -> Self {
+        let auto_despawn = std::env::var("AUTODESPAWN")
+            .or_else(|_| std::env::var("AUTOSPAWN"))
+            .map_or(true, |v| v.eq_ignore_ascii_case("true"));
+
+        let should_despawn = auto_despawn && !was_running;
+        Self {
+            local_config,
+            test_name,
+            should_despawn,
+        }
+    }
+
+    pub fn disarm_and_stop(mut self) -> Result<()> {
+        if self.should_despawn {
+            self.should_despawn = false;
+            super::stop::exec(self.local_config, self.test_name)?;
+        }
+        Ok(())
+    }
+}
+
+impl Drop for DespawnGuard<'_> {
+    fn drop(&mut self) {
+        if self.should_despawn {
+            let _ = super::stop::exec(self.local_config, self.test_name);
+        }
+    }
+}
+
 pub fn exec(
     local_config: ComposeTestLocalConfig,
     integration: &str,
@@ -39,7 +85,10 @@ pub fn exec(
     }
 
     let mut ran_environments = Vec::new();
+    let is_running = active.is_some();
     for environment in environments {
+        let despawn_guard = DespawnGuard::new(local_config, integration, is_running);
+
         run_environment(
             local_config,
             integration,
@@ -51,6 +100,7 @@ pub fn exec(
         if coverage {
             ran_environments.push(environment.clone());
         }
+        despawn_guard.disarm_and_stop()?;
     }
 
     if coverage {