diff --git a/src/server.test.ts b/src/server.test.ts
index 59bcc5d37..8979b831f 100644
--- a/src/server.test.ts
+++ b/src/server.test.ts
@@ -632,7 +632,13 @@ test("server shutdown waits for an active MCP tool call", async (t) => {
   assert.equal(shutdownFinished, false);
 
   await writeFile(join(root, "release"), "");
-  await toolCall;
+  const response = await toolCall;
+  assert.equal(response.status, 200, await response.clone().text());
+  const responseBody = await response.json() as {
+    result?: { structuredContent?: { exit_code?: number; running?: boolean } };
+  };
+  assert.equal(responseBody.result?.structuredContent?.exit_code, 0);
+  assert.equal(responseBody.result?.structuredContent?.running, false);
   await shutdown;
   assert.equal(shutdownFinished, true);
 });
diff --git a/src/server.ts b/src/server.ts
index 0a2792f3f..58496d27a 100644
--- a/src/server.ts
+++ b/src/server.ts
@@ -966,6 +966,12 @@ export function createServer(
     localAgentProviders,
     close: () => {
       closePromise ??= (async () => {
+        await toolActivities.waitForIdle();
+        // Tool handlers resolving only starts the JSON-RPC response chain;
+        // it settles several microtasks later. Yield to the macrotask queue
+        // so in-flight responses are delivered before mcpHandler.close()
+        // rejects their still-open exchanges (HTTP 499).
+        await new Promise<void>((resolve) => setImmediate(resolve));
         try {
           await mcpHandler.close();
         } catch (error) {
@@ -973,7 +979,6 @@ export function createServer(
             error: error instanceof Error ? error.message : String(error),
           });
         }
-        await toolActivities.waitForIdle();
         processSessions.shutdown();
         oauthProvider.close();
         workspaceStore.close?.();