diff --git a/apps/desktop/src/main/__tests__/runtime-host-collaboration-ipc-main.test.ts b/apps/desktop/src/main/__tests__/runtime-host-collaboration-ipc-main.test.ts
index 3da977f0a2..a161321e20 100644
--- a/apps/desktop/src/main/__tests__/runtime-host-collaboration-ipc-main.test.ts
+++ b/apps/desktop/src/main/__tests__/runtime-host-collaboration-ipc-main.test.ts
@@ -165,9 +165,11 @@ function peerReachability() {
 
 test('treats an unavailable collaboration authority as an empty background inbox', async () => {
   const handlers = new Map<string, IpcHandler>();
+  let queryCalls = 0;
   registerRuntimeHostCollaborationIpc(
     {
       async queryCollaborationTurnRequests() {
+        queryCalls += 1;
         throw new RuntimeHostOperationError(
           'collaboration.turn-request.query',
           'operation_unavailable',
@@ -191,6 +193,11 @@ test('treats an unavailable collaboration authority as an empty background inbox
     canRequestTurns: false,
     requests: [],
   });
+  assert.deepEqual(await query({} as Parameters<IpcHandler>[0]), {
+    canRequestTurns: false,
+    requests: [],
+  });
+  assert.equal(queryCalls, 1);
   await assert.rejects(
     query({} as Parameters<IpcHandler>[0], 'session-1'),
     RuntimeHostOperationError,
diff --git a/apps/desktop/src/main/runtime-host-collaboration-ipc-main.ts b/apps/desktop/src/main/runtime-host-collaboration-ipc-main.ts
index 502d5b9b23..47e5a677fc 100644
--- a/apps/desktop/src/main/runtime-host-collaboration-ipc-main.ts
+++ b/apps/desktop/src/main/runtime-host-collaboration-ipc-main.ts
@@ -46,6 +46,7 @@ export function registerRuntimeHostCollaborationIpc(
     | DesktopCollaborationConnectionTarget
     | Promise<DesktopCollaborationConnectionTarget>,
 ): void {
+  let backgroundInboxUnavailable = false;
   ipcMain.handle(
     'session-collaboration:prepare',
     async (
@@ -97,10 +98,14 @@ export function registerRuntimeHostCollaborationIpc(
     async (_event, sessionId: unknown) => {
       const requestedSessionId =
         sessionId === undefined ? undefined : requiredId(sessionId, 'Session');
+      if (requestedSessionId === undefined && backgroundInboxUnavailable) {
+        return { canRequestTurns: false, requests: [] };
+      }
       try {
         return await client.queryCollaborationTurnRequests(requestedSessionId);
       } catch (error) {
         if (requestedSessionId === undefined && isCollaborationInboxUnavailable(error)) {
+          backgroundInboxUnavailable = true;
           return { canRequestTurns: false, requests: [] };
         }
         throw error;