diff --git a/packages/angular/build/src/tools/vite/plugins/angular-memory-plugin.ts b/packages/angular/build/src/tools/vite/plugins/angular-memory-plugin.ts
index dc83f131f299..92fd7ac7df54 100644
--- a/packages/angular/build/src/tools/vite/plugins/angular-memory-plugin.ts
+++ b/packages/angular/build/src/tools/vite/plugins/angular-memory-plugin.ts
@@ -8,7 +8,7 @@
 
 import assert from 'node:assert';
 import { readFile } from 'node:fs/promises';
-import { dirname, join, relative } from 'node:path';
+import { basename, dirname, join, relative } from 'node:path';
 import type { Plugin } from 'vite';
 import { loadEsmModule } from '../../../utils/load-esm';
 import { AngularMemoryOutputFiles } from '../utils';
@@ -51,6 +51,18 @@ export async function createAngularMemoryPlugin(
           // Remove query if present
           const [importerFile] = importer.split('?', 1);
           source = '/' + join(dirname(relative(virtualProjectRoot, importerFile)), source);
+        } else if (
+          !ssr &&
+          source[0] === '/' &&
+          importer.endsWith('index.html') &&
+          normalizePath(importer).startsWith(virtualProjectRoot)
+        ) {
+          // This is only needed when using SSR and `angularSsrMiddleware` (old style) to correctly resolve
+          // .js files when using lazy-loading.
+          // Remove query if present
+          const [importerFile] = importer.split('?', 1);
+          source =
+            '/' + join(dirname(relative(virtualProjectRoot, importerFile)), basename(source));
         }
       }
 
diff --git a/tests/legacy-cli/e2e/tests/vite/ssr-no-server-entry-sub-path.ts b/tests/legacy-cli/e2e/tests/vite/ssr-no-server-entry-sub-path.ts
new file mode 100644
index 000000000000..a55f48d0b39f
--- /dev/null
+++ b/tests/legacy-cli/e2e/tests/vite/ssr-no-server-entry-sub-path.ts
@@ -0,0 +1,53 @@
+import assert from 'node:assert';
+import {
+  execAndWaitForOutputToMatch,
+  ng,
+  silentNg,
+  waitForAnyProcessOutputToMatch,
+} from '../../utils/process';
+import { installWorkspacePackages, uninstallPackage } from '../../utils/packages';
+import { useSha } from '../../utils/project';
+import { getGlobalVariable } from '../../utils/env';
+import { findFreePort } from '../../utils/network';
+import { writeFile } from '../../utils/fs';
+
+export default async function () {
+  assert(
+    getGlobalVariable('argv')['esbuild'],
+    'This test should not be called in the Webpack suite.',
+  );
+
+  // Forcibly remove in case another test doesn't clean itself up.
+  await uninstallPackage('@angular/ssr');
+  await ng('add', '@angular/ssr', '--no-server-routing', '--skip-confirmation', '--skip-install');
+  await useSha();
+  await installWorkspacePackages();
+
+  await silentNg('generate', 'component', 'home');
+  await writeFile(
+    'src/app/app.routes.ts',
+    `
+    import { Routes } from '@angular/router';
+    import {HomeComponent} from './home/home.component';
+
+    export const routes: Routes = [{
+      path: 'sub/home',
+      component: HomeComponent
+    }];
+    `,
+  );
+
+  const port = await findFreePort();
+  await execAndWaitForOutputToMatch('ng', ['serve', '--port', `${port}`], /complete/, {
+    NO_COLOR: 'true',
+  });
+
+  const [, response] = await Promise.all([
+    assert.rejects(
+      waitForAnyProcessOutputToMatch(/Pre-transform error: Failed to load url/, 8_000),
+    ),
+    fetch(`http://localhost:${port}/sub/home`),
+  ]);
+
+  assert(response.ok, `Expected 'response.ok' to be 'true'.`);
+}