diff --git a/packages/server/src/server/agent/providers/claude-agent.test.ts b/packages/server/src/server/agent/providers/claude-agent.test.ts
index f4363b62b3..450ec4b969 100644
--- a/packages/server/src/server/agent/providers/claude-agent.test.ts
+++ b/packages/server/src/server/agent/providers/claude-agent.test.ts
@@ -1,5 +1,5 @@
 import { describe, expect, test, vi } from "vitest";
-import type { ModelInfo } from "@anthropic-ai/claude-agent-sdk";
+import type { ModelInfo, SDKUserMessage } from "@anthropic-ai/claude-agent-sdk";
 
 import { createTestLogger } from "../../../test-utils/test-logger.js";
 import { ClaudeAgentClient, convertClaudeHistoryEntry } from "./claude-agent.js";
@@ -357,4 +357,52 @@ describe("ClaudeAgentClient.listModels", () => {
     ]);
     expect(queryMock.return).toHaveBeenCalledTimes(1);
   });
+
+  test("keeps the Claude control-plane query open until supportedModels resolves", async () => {
+    const queryMock = createSupportedModelsQueryMock([
+      {
+        value: "default",
+        displayName: "Default (recommended)",
+        description: "Sonnet 4.6 · Best for everyday tasks",
+      },
+    ] satisfies ModelInfo[]);
+    let promptIterator: AsyncIterator<SDKUserMessage, void> | null = null;
+    let promptNextPromise: Promise<IteratorResult<SDKUserMessage, void>> | null = null;
+    let promptClosedBeforeModelsResolved = false;
+
+    queryMock.supportedModels = vi.fn(async () => {
+      promptNextPromise = promptIterator?.next() ?? null;
+      if (!promptNextPromise) {
+        throw new Error("Prompt iterator not captured");
+      }
+      promptNextPromise.then(() => {
+        promptClosedBeforeModelsResolved = true;
+      });
+      await Promise.resolve();
+      expect(promptClosedBeforeModelsResolved).toBe(false);
+      return [
+        {
+          value: "default",
+          displayName: "Default (recommended)",
+          description: "Sonnet 4.6 · Best for everyday tasks",
+        },
+      ] satisfies ModelInfo[];
+    });
+
+    const queryFactory = vi.fn(({ prompt }) => {
+      promptIterator = prompt[Symbol.asyncIterator]();
+      return queryMock;
+    });
+    const client = new ClaudeAgentClient({
+      logger,
+      queryFactory: queryFactory as never,
+    });
+
+    const models = await client.listModels({ cwd: process.cwd() });
+
+    expect(models).toHaveLength(1);
+    expect(promptNextPromise).not.toBeNull();
+    await expect(promptNextPromise).resolves.toEqual({ done: true, value: undefined });
+    expect(queryMock.return).toHaveBeenCalledTimes(1);
+  });
 });
diff --git a/packages/server/src/server/agent/providers/claude-agent.ts b/packages/server/src/server/agent/providers/claude-agent.ts
index e38b2379a2..6a13d5bf67 100644
--- a/packages/server/src/server/agent/providers/claude-agent.ts
+++ b/packages/server/src/server/agent/providers/claude-agent.ts
@@ -225,10 +225,6 @@ function applyRuntimeSettingsToClaudeOptions(
   };
 }
 
-function createEmptyClaudePrompt(): AsyncGenerator<SDKUserMessage, void, undefined> {
-  return (async function* empty() {})();
-}
-
 function isClaudeThinkingEffort(value: string | null | undefined): value is ClaudeThinkingEffort {
   return value === "low" || value === "medium" || value === "high" || value === "max";
 }
@@ -1032,8 +1028,9 @@ export class ClaudeAgentClient implements AgentClient {
   }
 
   async listModels(options?: ListModelsOptions): Promise<AgentModelDefinition[]> {
+    const input = createAsyncMessageInput<SDKUserMessage>();
     const claudeQuery = this.queryFactory({
-      prompt: createEmptyClaudePrompt(),
+      prompt: input.iterable,
       options: applyRuntimeSettingsToClaudeOptions(
         {
           cwd: options?.cwd ?? process.cwd(),
@@ -1052,13 +1049,13 @@ export class ClaudeAgentClient implements AgentClient {
       this.logger.warn({ err: error }, "Failed to query Claude supportedModels()");
       throw error;
     } finally {
+      input.end();
       try {
         await claudeQuery.return?.();
       } catch {
         // ignore control-plane shutdown errors
       }
     }
-
   }
 
   async listPersistedAgents(