diff --git a/packages/cli/src/ui/AppContainer.test.tsx b/packages/cli/src/ui/AppContainer.test.tsx
index d37f3961ce7..9e409e04b02 100644
--- a/packages/cli/src/ui/AppContainer.test.tsx
+++ b/packages/cli/src/ui/AppContainer.test.tsx
@@ -1811,6 +1811,17 @@ describe('AppContainer State Management', () => {
     });
 
     it('restores the prompt when onCancelSubmit is called with shouldRestorePrompt=true (or undefined)', async () => {
+      // Mock history containing the message we want to restore
+      const mockHistory = [{ type: 'user', text: 'previous message' }];
+      mockedUseHistory.mockReturnValue({
+        history: mockHistory,
+        addItem: vi.fn(),
+        updateItem: vi.fn(),
+        clearItems: vi.fn(),
+        loadHistory: vi.fn(),
+      });
+
+      // Mock logger to return the same message so userMessages is populated
       mockedUseLogger.mockReturnValue({
         getPreviousUserMessages: vi
           .fn()
@@ -1818,6 +1829,8 @@ describe('AppContainer State Management', () => {
       });
 
       const { unmount } = renderAppContainer();
+
+      // Wait for userMessages to be populated
       await waitFor(() =>
         expect(capturedUIState.userMessages).toContain('previous message'),
       );
@@ -1826,11 +1839,15 @@ describe('AppContainer State Management', () => {
         mockedUseGeminiStream.mock.lastCall!,
       );
 
-      await act(async () => {
+      // Trigger cancel/restore
+      act(() => {
         onCancelSubmit(true);
       });
 
-      expect(mockSetText).toHaveBeenCalledWith('previous message');
+      // Wait for the effect to run and restore the text
+      await waitFor(() => {
+        expect(mockSetText).toHaveBeenCalledWith('previous message');
+      });
 
       unmount();
     });
diff --git a/packages/cli/src/ui/AppContainer.tsx b/packages/cli/src/ui/AppContainer.tsx
index ee2c18d1a27..ac41577a5dd 100644
--- a/packages/cli/src/ui/AppContainer.tsx
+++ b/packages/cli/src/ui/AppContainer.tsx
@@ -187,6 +187,8 @@ export const AppContainer = (props: AppContainerProps) => {
   const [warningBannerText, setWarningBannerText] = useState('');
   const [bannerVisible, setBannerVisible] = useState(true);
 
+  const [pendingPromptRestore, setPendingPromptRestore] = useState(false);
+
   const extensionManager = config.getExtensionLoader() as ExtensionManager;
   // We are in the interactive CLI, update how we request consent and settings.
   extensionManager.setRequestConsent((description) =>
@@ -725,8 +727,15 @@ Logging in with Google... Please restart Gemini CLI to continue.
         return;
       }
 
-      const lastUserMessage = userMessages.at(-1);
-      let textToSet = shouldRestorePrompt ? lastUserMessage || '' : '';
+      let textToSet = '';
+      if (shouldRestorePrompt) {
+        // Defer restoration to useEffect to ensure we get the latest user message
+        setPendingPromptRestore(true);
+        return;
+      }
+
+      // If we are not restoring, ensure we cancel any pending restore
+      setPendingPromptRestore(false);
 
       const queuedText = getQueuedMessagesText();
       if (queuedText) {
@@ -740,7 +749,6 @@ Logging in with Google... Please restart Gemini CLI to continue.
     },
     [
       buffer,
-      userMessages,
       getQueuedMessagesText,
       clearQueue,
       pendingSlashCommandHistoryItems,
@@ -748,6 +756,31 @@ Logging in with Google... Please restart Gemini CLI to continue.
     ],
   );
 
+  useEffect(() => {
+    if (pendingPromptRestore) {
+      // Check if userMessages is up to date with historyManager
+      const lastHistoryItem = historyManager.history.findLast(
+        (item) => item.type === 'user' && item.text,
+      );
+      const lastUserMessage = userMessages.at(-1);
+
+      if (
+        lastHistoryItem &&
+        lastHistoryItem.text === lastUserMessage &&
+        lastUserMessage
+      ) {
+        buffer.setText(lastUserMessage);
+        setPendingPromptRestore(false);
+      }
+    }
+  }, [
+    pendingPromptRestore,
+    userMessages,
+    historyManager.history,
+    buffer,
+    setPendingPromptRestore,
+  ]);
+
   const handleFinalSubmit = useCallback(
     (submittedValue: string) => {
       addMessage(submittedValue);