diff --git a/dev/src/server/adk_api_server.ts b/dev/src/server/adk_api_server.ts
index dd74b1290..5c756a760 100644
--- a/dev/src/server/adk_api_server.ts
+++ b/dev/src/server/adk_api_server.ts
@@ -346,7 +346,7 @@ export class AdkApiServer {
 
           const functionCalls = getFunctionCalls(event);
           const functionResponses = getFunctionResponses(event);
-          await using agentFile = await this.agentLoader.getAgentFile(appName);
+          const agentFile = await this.agentLoader.getAgentFile(appName);
           const loaded = await agentFile.load();
           const rootAgent = isApp(loaded) ? loaded.rootAgent : loaded;
 
@@ -1046,9 +1046,7 @@ export class AdkApiServer {
     runConfig?: RunConfig;
     abortSignal: AbortSignal;
   }): AsyncGenerator<Event> {
-    await using agentFile = await this.agentLoader.getAgentFile(
-      options.appName,
-    );
+    const agentFile = await this.agentLoader.getAgentFile(options.appName);
     const loaded = await agentFile.load();
     const runner = await this.getRunner(loaded, options.appName);
 
diff --git a/dev/src/utils/agent_loader.ts b/dev/src/utils/agent_loader.ts
index d5097c482..674f9d785 100644
--- a/dev/src/utils/agent_loader.ts
+++ b/dev/src/utils/agent_loader.ts
@@ -420,18 +420,29 @@ export class AgentLoader {
   }
 
   /**
-   * Disposes all cached agents and marks them for reload on the next request.
+   * Empties the cache and hands back the `AgentFile`s it held, so the caller
+   * can end their lives. The next `getAgentFile()` re-scans the agents
+   * directory.
    */
-  private invalidateAll(): void {
-    for (const agentFile of Object.values(this.preloadedAgents)) {
-      agentFile.dispose().catch(() => {});
-    }
+  private takeAgentFiles(): AgentFile[] {
+    const agentFiles = Object.values(this.preloadedAgents);
 
     for (const key of Object.keys(this.preloadedAgents)) {
       delete this.preloadedAgents[key];
     }
 
     this.agentsAlreadyPreloaded = false;
+
+    return agentFiles;
+  }
+
+  /**
+   * Disposes all cached agents and marks them for reload on the next request.
+   */
+  private invalidateAll(): void {
+    for (const agentFile of this.takeAgentFiles()) {
+      agentFile.dispose().catch(() => {});
+    }
   }
 
   async listAgents(): Promise<string[]> {
@@ -458,6 +469,14 @@ export class AgentLoader {
     return appNames.sort();
   }
 
+  /**
+   * Lends the caller the `AgentFile` this loader owns for `agentName`.
+   *
+   * Every caller shares one handle and must not dispose it: disposal deletes
+   * the compiled artifact and the temp directory the other callers still read
+   * from. Only `invalidateAll()` and `disposeAll()` end a handle's life, and
+   * both drop the cache entry with it.
+   */
   async getAgentFile(agentName: string): Promise<AgentFile> {
     await this.preloadAgents();
 
@@ -468,12 +487,15 @@ export class AgentLoader {
     return this.getAgentFile(appName);
   }
 
+  /**
+   * Disposes every `AgentFile` this loader owns and empties its cache, so a
+   * later `getAgentFile()` re-scans instead of lending a disposed handle.
+   */
   async disposeAll(): Promise<void> {
     this.watcher?.close();
     this.watcher = undefined;
-    await Promise.all(
-      Object.values(this.preloadedAgents).map((f) => f.dispose()),
-    );
+
+    await Promise.all(this.takeAgentFiles().map((f) => f.dispose()));
   }
 
   async preloadAgents() {
diff --git a/dev/test/server/adk_api_server_test.ts b/dev/test/server/adk_api_server_test.ts
index 6f464992e..81fab11c1 100644
--- a/dev/test/server/adk_api_server_test.ts
+++ b/dev/test/server/adk_api_server_test.ts
@@ -6,6 +6,7 @@
 
 import {AGENT_CARD_PATH, AgentCard} from '@a2a-js/sdk';
 import {
+  BaseAgent,
   BaseArtifactService,
   BaseMemoryService,
   BaseSessionService,
@@ -29,7 +30,7 @@ import {
   A2A_AUTH_TOKEN_ENV_VAR,
   AdkApiServer,
 } from '../../src/server/adk_api_server.js';
-import {AgentLoader} from '../../src/utils/agent_loader.js';
+import {AgentFile, AgentLoader} from '../../src/utils/agent_loader.js';
 
 interface JsonRpcResponse {
   result?: unknown;
@@ -213,6 +214,74 @@ const TEST_AGENT = new TestAgent({
   ],
 });
 
+const GRAPH_PATH =
+  '/apps/testApp/users/testUser/sessions/fullSession/events/event1/graph';
+
+/** An `AgentFile` that lends `TEST_AGENT` and counts how often it is disposed. */
+class CountingAgentFile extends AgentFile {
+  disposeCount = 0;
+
+  constructor() {
+    super('testApp.ts');
+  }
+
+  override load(): Promise<BaseAgent> {
+    return Promise.resolve(TEST_AGENT);
+  }
+
+  override dispose(): Promise<void> {
+    this.disposeCount++;
+
+    return Promise.resolve();
+  }
+}
+
+/** A session holding one event with a function call, for the graph endpoint. */
+function createGraphSession(): Session {
+  return createSession({
+    id: 'fullSession',
+    appName: 'testApp',
+    userId: 'testUser',
+    events: [
+      createEvent({
+        id: 'event1',
+        author: 'model',
+        content: {parts: [{functionCall: {name: 'foo', args: {}}}]},
+        invocationId: 'inv-1',
+      }),
+    ],
+  });
+}
+
+/** Runs the test agent once and reports the HTTP status. */
+async function postRun(client: HttpClient): Promise<number> {
+  const response = await client.post<Event[]>('/run', {
+    appName: 'testApp',
+    userId: 'testUser',
+    sessionId: 'sessionId',
+    newMessage: {parts: [{text: 'Hello test agent!'}], role: 'user'},
+  });
+
+  return response.status;
+}
+
+/** Fetches the event graph once and reports the HTTP status. */
+async function getEventGraph(
+  client: HttpClient,
+  sessionService: BaseSessionService,
+): Promise<number> {
+  const originalGetSession = sessionService.getSession;
+  sessionService.getSession = () => Promise.resolve(createGraphSession());
+
+  try {
+    const response = await client.get<{dotSrc: string}>(GRAPH_PATH);
+
+    return response.status;
+  } finally {
+    sessionService.getSession = originalGetSession;
+  }
+}
+
 describe('AdkWebServer', () => {
   let agentLoader: AgentLoader;
   let sessionService: BaseSessionService;
@@ -943,6 +1012,48 @@ describe('AdkWebServer', () => {
     });
   });
 
+  describe('agent file lifecycle', () => {
+    let agentFile: CountingAgentFile;
+    let originalGetAgentFile: AgentLoader['getAgentFile'];
+
+    beforeEach(async () => {
+      agentFile = new CountingAgentFile();
+      originalGetAgentFile = agentLoader.getAgentFile;
+      agentLoader.getAgentFile = () => Promise.resolve(agentFile);
+
+      await sessionService.createSession({
+        appName: 'testApp',
+        userId: 'testUser',
+        sessionId: 'sessionId',
+      });
+    });
+
+    afterEach(() => {
+      agentLoader.getAgentFile = originalGetAgentFile;
+    });
+
+    it('leaves the borrowed agent file undisposed across two sequential run requests', async () => {
+      expect(await postRun(client)).toBe(200);
+      expect(await postRun(client)).toBe(200);
+
+      expect(agentFile.disposeCount).toBe(0);
+    });
+
+    it('leaves the borrowed agent file undisposed across two sequential agent-graph requests', async () => {
+      expect(await getEventGraph(client, sessionService)).toBe(200);
+      expect(await getEventGraph(client, sessionService)).toBe(200);
+
+      expect(agentFile.disposeCount).toBe(0);
+    });
+
+    it('does not dispose the borrowed agent file when a run and a graph request share an app', async () => {
+      expect(await postRun(client)).toBe(200);
+      expect(await getEventGraph(client, sessionService)).toBe(200);
+
+      expect(agentFile.disposeCount).toBe(0);
+    });
+  });
+
   describe('A2A', () => {
     const A2A_TOKEN = 'test-a2a-token';
     let a2aServer: AdkApiServer | undefined;
diff --git a/dev/test/utils/agent_loader_test.ts b/dev/test/utils/agent_loader_test.ts
index 2285df895..3313e1c4c 100644
--- a/dev/test/utils/agent_loader_test.ts
+++ b/dev/test/utils/agent_loader_test.ts
@@ -717,6 +717,38 @@ describe('AgentLoader', () => {
       await agentLoader.disposeAll();
     });
 
+    it('lends the same live AgentFile to repeated getAgentFile calls', async () => {
+      const loader = new AgentLoader(tempAgentsDir);
+      const first = await loader.getAgentFile('agent2');
+      const second = await loader.getAgentFile('agent2');
+
+      expect(second).toBe(first);
+
+      await first.load();
+      await expect(fs.access(first.getFilePath())).resolves.toBeUndefined();
+
+      await loader.disposeAll();
+    });
+
+    it('re-scans and lends a fresh AgentFile after disposeAll', async () => {
+      const loader = new AgentLoader(tempAgentsDir);
+      await loader.listAgents();
+      const before = await loader.getAgentFile('agent2');
+      await before.load();
+      const beforePath = before.getFilePath();
+
+      await loader.disposeAll();
+      await expect(fs.access(beforePath)).rejects.toThrow();
+
+      const after = await loader.getAgentFile('agent2');
+
+      expect(after).not.toBe(before);
+      await expect(after.load()).resolves.toBeDefined();
+      await expect(fs.access(after.getFilePath())).resolves.toBeUndefined();
+
+      await loader.disposeAll();
+    });
+
     it('disposes all agent files', async () => {
       const agentLoader = new AgentLoader(tempAgentsDir);
       await agentLoader.listAgents();