diff --git a/goldens/circular-deps/packages.json b/goldens/circular-deps/packages.json
index 0d4d97ad1edd..96a53f7a1040 100644
--- a/goldens/circular-deps/packages.json
+++ b/goldens/circular-deps/packages.json
@@ -7,7 +7,6 @@
     "packages/angular/build/src/tools/esbuild/angular/component-stylesheets.ts",
     "packages/angular/build/src/tools/esbuild/bundler-context.ts",
     "packages/angular/build/src/tools/esbuild/utils.ts",
-    "packages/angular/build/src/utils/server-rendering/manifest.ts",
     "packages/angular/build/src/tools/esbuild/bundler-execution-result.ts"
   ],
   [
@@ -17,16 +16,18 @@
   [
     "packages/angular/build/src/tools/esbuild/bundler-context.ts",
     "packages/angular/build/src/tools/esbuild/utils.ts",
-    "packages/angular/build/src/utils/server-rendering/manifest.ts"
+    "packages/angular/build/src/tools/esbuild/bundler-execution-result.ts"
   ],
   [
     "packages/angular/build/src/tools/esbuild/bundler-context.ts",
     "packages/angular/build/src/tools/esbuild/utils.ts",
-    "packages/angular/build/src/utils/server-rendering/manifest.ts",
-    "packages/angular/build/src/tools/esbuild/bundler-execution-result.ts"
+    "packages/angular/build/src/utils/server-rendering/manifest.ts"
   ],
   [
     "packages/angular/build/src/tools/esbuild/bundler-execution-result.ts",
+    "packages/angular/build/src/tools/esbuild/utils.ts"
+  ],
+  [
     "packages/angular/build/src/tools/esbuild/utils.ts",
     "packages/angular/build/src/utils/server-rendering/manifest.ts"
   ],
diff --git a/packages/angular/build/src/builders/application/execute-post-bundle.ts b/packages/angular/build/src/builders/application/execute-post-bundle.ts
index bb2fb2e17b4d..bf23df37688b 100644
--- a/packages/angular/build/src/builders/application/execute-post-bundle.ts
+++ b/packages/angular/build/src/builders/application/execute-post-bundle.ts
@@ -40,6 +40,7 @@ import { OutputMode } from './schema';
  * @param initialFiles A map containing initial file information for the executed build.
  * @param locale A language locale to insert in the index.html.
  */
+// eslint-disable-next-line max-lines-per-function
 export async function executePostBundleSteps(
   options: NormalizedApplicationBuildOptions,
   outputFiles: BuildOutputFile[],
@@ -107,16 +108,19 @@ export async function executePostBundleSteps(
 
   // Create server manifest
   if (serverEntryPoint) {
+    const { manifestContent, serverAssetsChunks } = generateAngularServerAppManifest(
+      additionalHtmlOutputFiles,
+      outputFiles,
+      optimizationOptions.styles.inlineCritical ?? false,
+      undefined,
+      locale,
+    );
+
     additionalOutputFiles.push(
+      ...serverAssetsChunks,
       createOutputFile(
         SERVER_APP_MANIFEST_FILENAME,
-        generateAngularServerAppManifest(
-          additionalHtmlOutputFiles,
-          outputFiles,
-          optimizationOptions.styles.inlineCritical ?? false,
-          undefined,
-          locale,
-        ),
+        manifestContent,
         BuildOutputFileType.ServerApplication,
       ),
     );
@@ -194,15 +198,24 @@ export async function executePostBundleSteps(
       const manifest = additionalOutputFiles.find((f) => f.path === SERVER_APP_MANIFEST_FILENAME);
       assert(manifest, `${SERVER_APP_MANIFEST_FILENAME} was not found in output files.`);
 
-      manifest.contents = new TextEncoder().encode(
-        generateAngularServerAppManifest(
-          additionalHtmlOutputFiles,
-          outputFiles,
-          optimizationOptions.styles.inlineCritical ?? false,
-          serializableRouteTreeNodeForManifest,
-          locale,
-        ),
+      const { manifestContent, serverAssetsChunks } = generateAngularServerAppManifest(
+        additionalHtmlOutputFiles,
+        outputFiles,
+        optimizationOptions.styles.inlineCritical ?? false,
+        serializableRouteTreeNodeForManifest,
+        locale,
       );
+
+      for (const chunk of serverAssetsChunks) {
+        const idx = additionalOutputFiles.findIndex(({ path }) => path === chunk.path);
+        if (idx === -1) {
+          additionalOutputFiles.push(chunk);
+        } else {
+          additionalOutputFiles[idx] = chunk;
+        }
+      }
+
+      manifest.contents = new TextEncoder().encode(manifestContent);
     }
   }
 
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 9d6510588ffa..1f5012b028f3 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 { basename, dirname, join, relative } from 'node:path';
+import { dirname, join, relative } from 'node:path';
 import type { Plugin } from 'vite';
 import { loadEsmModule } from '../../../utils/load-esm';
 import { AngularMemoryOutputFiles } from '../utils';
@@ -24,8 +24,6 @@ export async function createAngularMemoryPlugin(
 ): Promise<Plugin> {
   const { virtualProjectRoot, outputFiles, external } = options;
   const { normalizePath } = await loadEsmModule<typeof import('vite')>('vite');
-  // See: https://github.com/vitejs/vite/blob/a34a73a3ad8feeacc98632c0f4c643b6820bbfda/packages/vite/src/node/server/pluginContainer.ts#L331-L334
-  const defaultImporter = join(virtualProjectRoot, 'index.html');
 
   return {
     name: 'vite:angular-memory',
@@ -40,16 +38,10 @@ export async function createAngularMemoryPlugin(
       }
 
       if (importer) {
-        let normalizedSource: string | undefined;
         if (source[0] === '.' && normalizePath(importer).startsWith(virtualProjectRoot)) {
           // Remove query if present
           const [importerFile] = importer.split('?', 1);
-          normalizedSource = join(dirname(relative(virtualProjectRoot, importerFile)), source);
-        } else if (source[0] === '/' && importer === defaultImporter) {
-          normalizedSource = basename(source);
-        }
-        if (normalizedSource) {
-          source = '/' + normalizePath(normalizedSource);
+          source = '/' + join(dirname(relative(virtualProjectRoot, importerFile)), source);
         }
       }
 
diff --git a/packages/angular/build/src/utils/server-rendering/manifest.ts b/packages/angular/build/src/utils/server-rendering/manifest.ts
index 1265bd110915..505eeb0ed516 100644
--- a/packages/angular/build/src/utils/server-rendering/manifest.ts
+++ b/packages/angular/build/src/utils/server-rendering/manifest.ts
@@ -11,8 +11,8 @@ import {
   NormalizedApplicationBuildOptions,
   getLocaleBaseHref,
 } from '../../builders/application/options';
-import type { BuildOutputFile } from '../../tools/esbuild/bundler-context';
-import type { PrerenderedRoutesRecord } from '../../tools/esbuild/bundler-execution-result';
+import { type BuildOutputFile, BuildOutputFileType } from '../../tools/esbuild/bundler-context';
+import { createOutputFile } from '../../tools/esbuild/utils';
 
 export const SERVER_APP_MANIFEST_FILENAME = 'angular-app-manifest.mjs';
 export const SERVER_APP_ENGINE_MANIFEST_FILENAME = 'angular-app-engine-manifest.mjs';
@@ -104,8 +104,9 @@ export default {
  * @param locale - An optional string representing the locale or language code to be used for
  * the application, helping with localization and rendering content specific to the locale.
  *
- * @returns A string representing the content of the SSR server manifest for the Node.js
- * environment.
+ * @returns An object containing:
+ * - `manifestContent`: A string of the SSR manifest content.
+ * - `serverAssetsChunks`: An array of build output files containing the generated assets for the server.
  */
 export function generateAngularServerAppManifest(
   additionalHtmlOutputFiles: Map<string, BuildOutputFile>,
@@ -113,13 +114,29 @@ export function generateAngularServerAppManifest(
   inlineCriticalCss: boolean,
   routes: readonly unknown[] | undefined,
   locale: string | undefined,
-): string {
+): {
+  manifestContent: string;
+  serverAssetsChunks: BuildOutputFile[];
+} {
+  const serverAssetsChunks: BuildOutputFile[] = [];
   const serverAssetsContent: string[] = [];
   for (const file of [...additionalHtmlOutputFiles.values(), ...outputFiles]) {
     const extension = extname(file.path);
     if (extension === '.html' || (inlineCriticalCss && extension === '.css')) {
+      const jsChunkFilePath = `assets-chunks/${file.path.replace(/[./]/g, '_')}.mjs`;
+      const escapedContent = escapeUnsafeChars(file.text);
+
+      serverAssetsChunks.push(
+        createOutputFile(
+          jsChunkFilePath,
+          `export default \`${escapedContent}\`;`,
+          BuildOutputFileType.ServerApplication,
+        ),
+      );
+
+      const contentLength = Buffer.byteLength(escapedContent);
       serverAssetsContent.push(
-        `['${file.path}', { size: ${file.size}, hash: '${file.hash}', text: async () => \`${escapeUnsafeChars(file.text)}\`}]`,
+        `['${file.path}', {size: ${contentLength}, hash: '${file.hash}', text: () => import('./${jsChunkFilePath}').then(m => m.default)}]`,
       );
     }
   }
@@ -129,10 +146,10 @@ export default {
   bootstrap: () => import('./main.server.mjs').then(m => m.default),
   inlineCriticalCss: ${inlineCriticalCss},
   routes: ${JSON.stringify(routes, undefined, 2)},
-  assets: new Map([${serverAssetsContent.join(', \n')}]),
+  assets: new Map([\n${serverAssetsContent.join(', \n')}\n]),
   locale: ${locale !== undefined ? `'${locale}'` : undefined},
 };
 `;
 
-  return manifestContent;
+  return { manifestContent, serverAssetsChunks };
 }