diff --git a/packages/@react-aria/utils/src/runAfterTransition.ts b/packages/@react-aria/utils/src/runAfterTransition.ts
index 1656cdf9030..3004d2313df 100644
--- a/packages/@react-aria/utils/src/runAfterTransition.ts
+++ b/packages/@react-aria/utils/src/runAfterTransition.ts
@@ -91,9 +91,25 @@ if (typeof document !== 'undefined') {
   }
 }
 
+/**
+ * Cleans up any elements that are no longer in the document.
+ * This is necessary because we can't rely on transitionend events to fire
+ * for elements that are removed from the document while transitioning.
+ */
+function cleanupDetachedElements() {
+  for (const [eventTarget] of transitionsByElement) {
+    // Similar to `eventTarget instanceof Element && !eventTarget.isConnected`, but avoids
+    // the explicit instanceof check, since it may be different in different contexts.
+    if ('isConnected' in eventTarget && !eventTarget.isConnected) {
+      transitionsByElement.delete(eventTarget);
+    }
+  }
+}
+
 export function runAfterTransition(fn: () => void): void {
   // Wait one frame to see if an animation starts, e.g. a transition on mount.
   requestAnimationFrame(() => {
+    cleanupDetachedElements();
     // If no transitions are running, call the function immediately.
     // Otherwise, add it to a list of callbacks to run at the end of the animation.
     if (transitionsByElement.size === 0) {
diff --git a/packages/@react-aria/utils/test/runAfterTransition.test.ts b/packages/@react-aria/utils/test/runAfterTransition.test.ts
new file mode 100644
index 00000000000..c0e67b5c260
--- /dev/null
+++ b/packages/@react-aria/utils/test/runAfterTransition.test.ts
@@ -0,0 +1,135 @@
+import {act} from '@testing-library/react';
+import {runAfterTransition} from '../src/runAfterTransition';
+
+class MockTransitionEvent extends Event {
+  propertyName: string;
+
+  constructor(type: string, eventInitDict?: TransitionEventInit) {
+    super(type, eventInitDict);
+    this.propertyName = eventInitDict?.propertyName || '';
+  }
+}
+
+describe('runAfterTransition', () => {
+  const originalTransitionEvent = global.TransitionEvent;
+  const nodes = new Set<Node>();
+
+  beforeAll(() => {
+    global.TransitionEvent = MockTransitionEvent as any;
+  });
+
+  afterAll(() => {
+    global.TransitionEvent = originalTransitionEvent;
+  });
+  
+  beforeEach(() => {
+    jest.useFakeTimers();
+  });
+
+  afterEach(() => {
+    jest.useRealTimers();
+    jest.restoreAllMocks();
+    cleanupElements();
+  });
+
+  function appendElement(element: HTMLElement) {
+    nodes.add(element);
+    document.body.appendChild(element);
+    return element;
+  }
+
+  function cleanupElements() {
+    for (const node of nodes) {
+      document.body.removeChild(node);
+      nodes.delete(node);
+    }
+  }
+
+  it('calls callback immediately when no transition is running', () => {
+    const callback = jest.fn();
+    runAfterTransition(callback);
+    act(() => {jest.runOnlyPendingTimers();});
+    expect(callback).toHaveBeenCalled();
+  });
+
+  it('defers callback until transition end when a transition is running', () => {
+    const element = appendElement(document.createElement('div'));
+
+    const callback = jest.fn();
+
+    element.dispatchEvent(
+      new TransitionEvent('transitionrun', {
+        propertyName: 'opacity',
+        bubbles: true
+      })
+    );
+
+    
+    runAfterTransition(callback);
+    act(() => {jest.runOnlyPendingTimers();});
+
+    // Callback should not be called immediately since a transition is active.
+    expect(callback).not.toHaveBeenCalled();
+
+    // Dispatch a transitionend event to finish the transition.
+    element.dispatchEvent(
+      new TransitionEvent('transitionend', {
+        propertyName: 'opacity',
+        bubbles: true
+      })
+    );
+    expect(callback).toHaveBeenCalled();
+  });
+
+  it('calls multiple queued callbacks after transition ends', () => {
+    const element = appendElement(document.createElement('div'));
+    const callback1 = jest.fn();
+    const callback2 = jest.fn();
+
+    element.dispatchEvent(
+      new TransitionEvent('transitionrun', {
+        propertyName: 'width',
+        bubbles: true
+      })
+    );
+
+    runAfterTransition(callback1);
+    act(() => {jest.runOnlyPendingTimers();});
+    runAfterTransition(callback2);
+    act(() => {jest.runOnlyPendingTimers();});
+    // Callbacks should not be called during transition.
+    expect(callback1).not.toHaveBeenCalled();
+    expect(callback2).not.toHaveBeenCalled();
+
+    element.dispatchEvent(
+      new TransitionEvent('transitionend', {
+        propertyName: 'width',
+        bubbles: true
+      })
+    );
+
+    expect(callback1).toHaveBeenCalled();
+    expect(callback2).toHaveBeenCalled();
+  });
+
+  it('clears out detached elements from transitionsByElement', () => {
+    const element = document.createElement('div');
+    element.id = 'test-element';
+    appendElement(element);
+    const callback = jest.fn();
+
+    element.dispatchEvent(
+      new TransitionEvent('transitionrun', {
+        propertyName: 'width',
+        bubbles: true
+      })
+    );
+
+    cleanupElements();
+
+    runAfterTransition(callback);
+    act(() => {jest.runOnlyPendingTimers();});
+
+    expect(callback).toHaveBeenCalled();
+  });
+});