diff --git a/packages/workspace-server/src/services/agent/agent.test.ts b/packages/workspace-server/src/services/agent/agent.test.ts
index 293ac3854e..14204e4065 100644
--- a/packages/workspace-server/src/services/agent/agent.test.ts
+++ b/packages/workspace-server/src/services/agent/agent.test.ts
@@ -845,6 +845,29 @@ describe("AgentService", () => {
       expect(prompt).toContain("If the user names a folder or path");
     });
   });
+
+  describe("system prompt questions", () => {
+    it("requires blocking questions to use a structured user-input tool", () => {
+      const prompt = (
+        service as unknown as {
+          buildSystemPrompt: (
+            credentials: { apiHost: string; projectId: number },
+            taskId: string,
+          ) => { append: string };
+        }
+      ).buildSystemPrompt(
+        { apiHost: "https://app.posthog.com", projectId: 1 },
+        "task-1",
+      ).append;
+
+      expect(prompt).toContain(
+        "use the structured user-input tool available in your current mode",
+      );
+      expect(prompt).toContain(
+        "plain-text questions mark the task as finished",
+      );
+    });
+  });
 });
 
 describe("buildAutoApproveOutcome", () => {
diff --git a/packages/workspace-server/src/services/agent/agent.ts b/packages/workspace-server/src/services/agent/agent.ts
index a352357e3b..9fa5c7db8a 100644
--- a/packages/workspace-server/src/services/agent/agent.ts
+++ b/packages/workspace-server/src/services/agent/agent.ts
@@ -652,6 +652,9 @@ When creating pull requests, add the following footer at the end of the PR descr
 
 When you mention a pull request in any reply or summary, always hyperlink it to its full URL (e.g. a Markdown link like [#123](https://github.com/org/repo/pull/123)) rather than plain text, so readers can open it directly.
 
+## Questions
+When you need an answer from the user before you can continue, use the structured user-input tool available in your current mode. Never end a turn with a blocking question in a normal assistant message because plain-text questions mark the task as finished instead of waiting for the user's response.
+
 ## Shell efficiency
 Optimize for the fewest shell round trips.
 - Batch related commands into one Bash invocation using \`&&\` (e.g. \`npm run typecheck && npm run lint && npm test\`).