diff --git a/site/src/pages/AgentsPage/AgentDetail/ChatContext.test.tsx b/site/src/pages/AgentsPage/AgentDetail/ChatContext.test.tsx
index b4244bb406..7a737e433d 100644
--- a/site/src/pages/AgentsPage/AgentDetail/ChatContext.test.tsx
+++ b/site/src/pages/AgentsPage/AgentDetail/ChatContext.test.tsx
@@ -797,6 +797,80 @@ describe("useChatStore", () => {
 		});
 	});
 
+	it("corrects stale queued messages from cache when switching back to a chat", async () => {
+		const chatID = "chat-1";
+		const existingMessage = makeMessage(chatID, 1, "user", "hello");
+		const queuedMessage = makeQueuedMessage(chatID, 10, "queued");
+		const mockSocket = createMockSocket();
+		vi.mocked(watchChat).mockReturnValue(mockSocket as never);
+
+		const queryClient = createTestQueryClient();
+		const wrapper = ({ children }: PropsWithChildren) => (
+			<QueryClientProvider client={queryClient}>{children}</QueryClientProvider>
+		);
+		const setChatErrorReason = vi.fn();
+		const clearChatErrorReason = vi.fn();
+
+		// Start with queued messages from a stale React Query cache.
+		// This simulates coming back to a chat whose queue was drained
+		// server-side while the user was viewing a different chat.
+		const staleOptions = {
+			chatID,
+			chatMessages: [existingMessage],
+			chatRecord: makeChat(chatID),
+			chatData: {
+				chat: makeChat(chatID),
+				messages: [existingMessage],
+				queued_messages: [queuedMessage],
+			},
+			chatQueuedMessages: [queuedMessage],
+			setChatErrorReason,
+			clearChatErrorReason,
+		};
+
+		const { result, rerender } = renderHook(
+			(options: Parameters<typeof useChatStore>[0]) => {
+				const { store } = useChatStore(options);
+				return {
+					queuedMessages: useChatSelector(store, selectQueuedMessages),
+				};
+			},
+			{
+				initialProps: staleOptions,
+				wrapper,
+			},
+		);
+
+		await waitFor(() => {
+			expect(watchChat).toHaveBeenCalledWith(chatID, 1);
+		});
+		// Initially shows the stale queued message from cache.
+		expect(result.current.queuedMessages.map((m) => m.id)).toEqual([
+			queuedMessage.id,
+		]);
+
+		// Simulate the REST query refetching and returning fresh
+		// data with an empty queue (no queue_update from WS yet).
+		rerender({
+			...staleOptions,
+			chatData: {
+				chat: {
+					...makeChat(chatID),
+					updated_at: "2025-01-01T00:00:02.000Z",
+				},
+				messages: [existingMessage],
+				queued_messages: [],
+			},
+			chatQueuedMessages: [],
+		});
+
+		// The store should accept the fresh REST data because the
+		// WebSocket hasn't sent a queue_update yet.
+		await waitFor(() => {
+			expect(result.current.queuedMessages).toEqual([]);
+		});
+	});
+
 	it("writes queue_update snapshots into the chat query cache", async () => {
 		const chatID = "chat-1";
 		const existingMessage = makeMessage(chatID, 1, "user", "hello");
diff --git a/site/src/pages/AgentsPage/AgentDetail/ChatContext.ts b/site/src/pages/AgentsPage/AgentDetail/ChatContext.ts
index 6c571d9b73..6217cd76f4 100644
--- a/site/src/pages/AgentsPage/AgentDetail/ChatContext.ts
+++ b/site/src/pages/AgentsPage/AgentDetail/ChatContext.ts
@@ -454,6 +454,13 @@ export const useChatStore = (
 	const storeRef = useRef<ChatStore>(createChatStore());
 	const streamResetFrameRef = useRef<number | null>(null);
 	const queuedMessagesHydratedChatIDRef = useRef<string | null>(null);
+	// Tracks whether the WebSocket has delivered a queue_update for the
+	// current chat. When true, the stream is the authoritative source
+	// and REST re-fetches must not overwrite the store. When false,
+	// REST data is allowed to re-hydrate so stale cached queued
+	// messages are corrected when switching back to a chat whose
+	// queue was drained while the user was away.
+	const wsQueueUpdateReceivedRef = useRef(false);
 	const activeChatIDRef = useRef<string | null>(null);
 	const prevChatIDRef = useRef<string | undefined>(chatID);
 
@@ -553,6 +560,7 @@ export const useChatStore = (
 
 	useEffect(() => {
 		queuedMessagesHydratedChatIDRef.current = null;
+		wsQueueUpdateReceivedRef.current = false;
 		store.setQueuedMessages([]);
 		if (!chatID) {
 			return;
@@ -563,7 +571,15 @@ export const useChatStore = (
 		if (!chatID || !chatData) {
 			return;
 		}
-		if (queuedMessagesHydratedChatIDRef.current === chatID) {
+		// Allow re-hydration from REST as long as the WebSocket hasn't
+		// delivered a queue_update yet (which would be fresher). This
+		// ensures that when the user navigates back to a chat whose
+		// queued messages were drained server-side while they were
+		// away, the REST refetch corrects the stale cached state.
+		if (
+			queuedMessagesHydratedChatIDRef.current === chatID &&
+			wsQueueUpdateReceivedRef.current
+		) {
 			return;
 		}
 		queuedMessagesHydratedChatIDRef.current = chatID;
@@ -688,6 +704,7 @@ export const useChatStore = (
 								continue;
 							}
 						}
+						wsQueueUpdateReceivedRef.current = true;
 						store.setQueuedMessages(streamEvent.queued_messages);
 						updateChatQueuedMessages(streamEvent.queued_messages);
 						continue;