diff --git a/packages/angular/ssr/src/app-engine.ts b/packages/angular/ssr/src/app-engine.ts
index 0ce5d23c30d1..dd204a4b595f 100644
--- a/packages/angular/ssr/src/app-engine.ts
+++ b/packages/angular/ssr/src/app-engine.ts
@@ -191,9 +191,10 @@ export class AngularAppEngine {
    * @returns A promise that resolves to the entry point exports or `undefined` if not found.
    */
   private getEntryPointExportsForUrl(url: URL): Promise<EntryPointExports> | undefined {
-    const { basePath } = this.manifest;
+    const { basePath, supportedLocales } = this.manifest;
+
     if (this.supportedLocales.length === 1) {
-      return this.getEntryPointExports('');
+      return this.getEntryPointExports(supportedLocales[this.supportedLocales[0]]);
     }
 
     const potentialLocale = getPotentialLocaleIdFromUrl(url, basePath);
diff --git a/packages/angular/ssr/src/manifest.ts b/packages/angular/ssr/src/manifest.ts
index 8fc415546033..0de603bba104 100644
--- a/packages/angular/ssr/src/manifest.ts
+++ b/packages/angular/ssr/src/manifest.ts
@@ -73,7 +73,7 @@ export interface AngularAppEngineManifest {
    * - `key`: The locale identifier (e.g., 'en', 'fr').
    * - `value`: The url segment associated with that locale.
    */
-  readonly supportedLocales: Readonly<Record<string, string | undefined>>;
+  readonly supportedLocales: Readonly<Record<string, string>>;
 }
 
 /**
diff --git a/packages/angular/ssr/test/app-engine_spec.ts b/packages/angular/ssr/test/app-engine_spec.ts
index 966edadce843..b08931b9400b 100644
--- a/packages/angular/ssr/test/app-engine_spec.ts
+++ b/packages/angular/ssr/test/app-engine_spec.ts
@@ -157,6 +157,66 @@ describe('AngularAppEngine', () => {
     });
   });
 
+  describe('Localized app with single locale', () => {
+    beforeAll(() => {
+      setAngularAppEngineManifest({
+        entryPoints: {
+          it: createEntryPoint('it'),
+        },
+        supportedLocales: { 'it': 'it' },
+        basePath: '/',
+      });
+
+      appEngine = new AngularAppEngine();
+    });
+
+    describe('handle', () => {
+      it('should return null for requests to unknown pages', async () => {
+        const request = new Request('https://example.com/unknown/page');
+        const response = await appEngine.handle(request);
+        expect(response).toBeNull();
+      });
+
+      it('should return a rendered page with correct locale', async () => {
+        const request = new Request('https://example.com/it/ssr');
+        const response = await appEngine.handle(request);
+        expect(await response?.text()).toContain('SSR works IT');
+      });
+
+      it('should correctly render the content when the URL ends with "index.html" with correct locale', async () => {
+        const request = new Request('https://example.com/it/ssr/index.html');
+        const response = await appEngine.handle(request);
+        expect(await response?.text()).toContain('SSR works IT');
+        expect(response?.headers?.get('Content-Language')).toBe('it');
+      });
+
+      it('should return a serve prerendered page with correct locale', async () => {
+        const request = new Request('https://example.com/it/ssg');
+        const response = await appEngine.handle(request);
+        expect(await response?.text()).toContain('SSG works IT');
+        expect(response?.headers?.get('Content-Language')).toBe('it');
+      });
+
+      it('should correctly serve the prerendered content when the URL ends with "index.html" with correct locale', async () => {
+        const request = new Request('https://example.com/it/ssg/index.html');
+        const response = await appEngine.handle(request);
+        expect(await response?.text()).toContain('SSG works IT');
+      });
+
+      it('should return null for requests to unknown pages in a locale', async () => {
+        const request = new Request('https://example.com/it/unknown/page');
+        const response = await appEngine.handle(request);
+        expect(response).toBeNull();
+      });
+
+      it('should return null for requests to file-like resources in a locale', async () => {
+        const request = new Request('https://example.com/it/logo.png');
+        const response = await appEngine.handle(request);
+        expect(response).toBeNull();
+      });
+    });
+  });
+
   describe('Non-localized app', () => {
     beforeAll(() => {
       @Component({