diff --git a/containers/api-proxy/copilot-byok.test.js b/containers/api-proxy/copilot-byok.test.js
index fc0ef6255..e17e63c15 100644
--- a/containers/api-proxy/copilot-byok.test.js
+++ b/containers/api-proxy/copilot-byok.test.js
@@ -195,6 +195,38 @@ describe('createCopilotAdapter — BYOK getAuthHeaders', () => {
     expect(config.apiVersion).toBe('2026-07-01');
   });
 
+  it.each([
+    ['/auto', '2026-08-01'],
+    ['/models/session', '2025-07-16'],
+    ['/models/session/intent', '2025-07-16'],
+  ])('injects the required API version for POST %s', (url, expectedVersion) => {
+    const adapter = createCopilotAdapter({ COPILOT_GITHUB_TOKEN: githubToken });
+    const headers = adapter.getAuthHeaders({ url, method: 'POST', headers: {} });
+
+    expect(headers['X-GitHub-Api-Version']).toBe(expectedVersion);
+  });
+
+  it('preserves a caller-supplied API version for /auto', () => {
+    const adapter = createCopilotAdapter({ COPILOT_GITHUB_TOKEN: githubToken });
+    const headers = adapter.getAuthHeaders({
+      url: '/auto',
+      method: 'POST',
+      headers: { 'x-github-api-version': '2027-01-01' },
+    });
+
+    expect(headers['X-GitHub-Api-Version']).toBeUndefined();
+  });
+
+  it('does not inject GitHub API versions into custom BYOK targets', () => {
+    const adapter = createCopilotAdapter({
+      COPILOT_PROVIDER_API_KEY: byokKey,
+      COPILOT_API_TARGET: 'router.example.com',
+    });
+    const headers = adapter.getAuthHeaders({ url: '/auto', method: 'POST', headers: {} });
+
+    expect(headers['X-GitHub-Api-Version']).toBeUndefined();
+  });
+
   it('uses COPILOT_PROVIDER_API_KEY (not COPILOT_GITHUB_TOKEN) for inference in BYOK+token mode', () => {
     const adapter = createCopilotAdapter({
       COPILOT_GITHUB_TOKEN: githubToken,
diff --git a/containers/api-proxy/providers/copilot.js b/containers/api-proxy/providers/copilot.js
index ab5617213..96cc1052f 100644
--- a/containers/api-proxy/providers/copilot.js
+++ b/containers/api-proxy/providers/copilot.js
@@ -34,12 +34,35 @@ const {
   resolveCopilotAuthToken,
   deriveCopilotApiTarget,
   copilotTargetRequiresGitHubTokenPrefix,
+  isGithubCopilotCatalogTarget,
 } = require('./copilot-auth');
 const { bearerAuthHeaders, withCopilotIntegration } = require('./auth-headers');
 const { URL } = require('url');
 const { COPILOT_ENV } = require('../provider-env-constants');
 
 const COPILOT_MODELS_API_VERSION = '2026-07-01';
+const COPILOT_LEGACY_AUTO_API_VERSION = '2025-07-16';
+const COPILOT_AUTO_API_VERSION = '2026-08-01';
+
+function hasRequestHeader(req, name) {
+  return Object.keys(req.headers || {}).some(header => header.toLowerCase() === name.toLowerCase());
+}
+
+function getDefaultAutoApiVersion(req, pathname, rawTarget) {
+  if (
+    req.method !== 'POST'
+    || hasRequestHeader(req, 'x-github-api-version')
+    || !isGithubCopilotCatalogTarget(rawTarget)
+  ) {
+    return undefined;
+  }
+
+  if (pathname === '/auto') return COPILOT_AUTO_API_VERSION;
+  if (pathname === '/models/session' || pathname === '/models/session/intent') {
+    return COPILOT_LEGACY_AUTO_API_VERSION;
+  }
+  return undefined;
+}
 
 /**
  * Create the GitHub Copilot provider adapter.
@@ -261,7 +284,12 @@ function createCopilotAdapter(env, deps = {}) {
         return withCopilotIntegration({ 'Authorization': prefix + ' ' + githubToken }, integrationId);
       }
 
-      return resolveHeaders();
+      const headers = resolveHeaders();
+      const autoApiVersion = getDefaultAutoApiVersion(req, reqPathname, rawTarget);
+      if (autoApiVersion) {
+        headers['X-GitHub-Api-Version'] = autoApiVersion;
+      }
+      return headers;
     },
   });
 }
diff --git a/containers/api-proxy/request-headers.test.js b/containers/api-proxy/request-headers.test.js
index 934bdceca..3677c8ae3 100644
--- a/containers/api-proxy/request-headers.test.js
+++ b/containers/api-proxy/request-headers.test.js
@@ -35,6 +35,8 @@ describe('request-headers', () => {
     const req = {
       headers: {
         'x-custom': 'keep-me',
+        'copilot-session-token': 'session-jwt',
+        'x-github-tenant': 'tenant-id',
         'transfer-encoding': 'chunked',
       },
     };
@@ -47,6 +49,8 @@ describe('request-headers', () => {
     });
 
     expect(headers['x-initiator']).toBe('agent');
+    expect(headers['copilot-session-token']).toBe('session-jwt');
+    expect(headers['x-github-tenant']).toBe('tenant-id');
     expect(headers['content-length']).toBe(String(body.length));
     expect(headers['transfer-encoding']).toBeUndefined();
   });