diff --git a/packages/angular/build/src/builders/application/execute-build.ts b/packages/angular/build/src/builders/application/execute-build.ts
index 51351c3aa3..d07e2a7937 100644
--- a/packages/angular/build/src/builders/application/execute-build.ts
+++ b/packages/angular/build/src/builders/application/execute-build.ts
@@ -240,11 +240,6 @@ export async function executeBuild(
     );
   }
 
-  // Override auto-CSP settings if we are serving through Vite middleware.
-  if (context.builder.builderName === 'dev-server' && options.security) {
-    options.security.autoCsp = false;
-  }
-
   // Perform i18n translation inlining if enabled
   if (i18nOptions.shouldInline) {
     const result = await inlineI18n(metafile, options, executionResult, initialFiles);
diff --git a/packages/angular/build/src/builders/application/options.ts b/packages/angular/build/src/builders/application/options.ts
index 17d5eb65a1..2c11e57aae 100644
--- a/packages/angular/build/src/builders/application/options.ts
+++ b/packages/angular/build/src/builders/application/options.ts
@@ -386,6 +386,15 @@ export async function normalizeOptions(
     }
   }
 
+  const autoCsp = options.security?.autoCsp;
+  const security = {
+    autoCsp: autoCsp
+      ? {
+          unsafeEval: autoCsp === true ? false : !!autoCsp.unsafeEval,
+        }
+      : undefined,
+  };
+
   // Initial options to keep
   const {
     allowedCommonJsDependencies,
@@ -415,7 +424,6 @@ export async function normalizeOptions(
     partialSSRBuild = false,
     externalRuntimeStyles,
     instrumentForCoverage,
-    security,
   } = options;
 
   // Return all the normalized options
diff --git a/packages/angular/build/src/builders/dev-server/vite-server.ts b/packages/angular/build/src/builders/dev-server/vite-server.ts
index 6773e8945c..4ca9925213 100644
--- a/packages/angular/build/src/builders/dev-server/vite-server.ts
+++ b/packages/angular/build/src/builders/dev-server/vite-server.ts
@@ -112,6 +112,11 @@ export async function* serveWithVite(
     browserOptions.ssr ||= true;
   }
 
+  // Disable auto CSP.
+  browserOptions.security = {
+    autoCsp: false,
+  };
+
   // Set all packages as external to support Vite's prebundle caching
   browserOptions.externalPackages = serverOptions.prebundle;
 
diff --git a/packages/angular/build/src/tools/esbuild/index-html-generator.ts b/packages/angular/build/src/tools/esbuild/index-html-generator.ts
index 4d11ed4fa4..4ccd48f2b5 100644
--- a/packages/angular/build/src/tools/esbuild/index-html-generator.ts
+++ b/packages/angular/build/src/tools/esbuild/index-html-generator.ts
@@ -80,15 +80,6 @@ export async function generateIndexHtml(
     throw new Error(`Output file does not exist: ${relativefilePath}`);
   };
 
-  // Read the Auto CSP options.
-  const autoCsp = buildOptions.security?.autoCsp;
-  const autoCspOptions =
-    autoCsp === true
-      ? { unsafeEval: false }
-      : autoCsp
-        ? { unsafeEval: !!autoCsp.unsafeEval }
-        : undefined;
-
   // Create an index HTML generator that reads from the in-memory output files
   const indexHtmlGenerator = new IndexHtmlGenerator({
     indexPath: indexHtmlOptions.input,
@@ -103,7 +94,7 @@ export async function generateIndexHtml(
       buildOptions.prerenderOptions ||
       buildOptions.appShellOptions
     ),
-    autoCsp: autoCspOptions,
+    autoCsp: buildOptions.security.autoCsp,
   });
 
   indexHtmlGenerator.readAsset = readAsset;
diff --git a/packages/angular/build/src/utils/index-file/auto-csp.ts b/packages/angular/build/src/utils/index-file/auto-csp.ts
index 8a5e339a9a..c50e0bfce3 100644
--- a/packages/angular/build/src/utils/index-file/auto-csp.ts
+++ b/packages/angular/build/src/utils/index-file/auto-csp.ts
@@ -98,7 +98,7 @@ export async function autoCsp(html: string, unsafeEval = false): Promise<string>
     scriptContent = [];
   }
 
-  rewriter.on('startTag', (tag, html) => {
+  rewriter.on('startTag', (tag) => {
     if (tag.tagName === 'script') {
       openedScriptTag = tag;
       const src = getScriptAttributeValue(tag, 'src');
diff --git a/packages/angular/build/src/utils/index-file/index-html-generator.ts b/packages/angular/build/src/utils/index-file/index-html-generator.ts
index 9bfb929c5d..52a926ef58 100644
--- a/packages/angular/build/src/utils/index-file/index-html-generator.ts
+++ b/packages/angular/build/src/utils/index-file/index-html-generator.ts
@@ -82,7 +82,7 @@ export class IndexHtmlGenerator {
 
     // CSR plugins
     if (options?.optimization?.styles?.inlineCritical) {
-      this.csrPlugins.push(inlineCriticalCssPlugin(this));
+      this.csrPlugins.push(inlineCriticalCssPlugin(this, !!options.autoCsp));
     }
 
     this.csrPlugins.push(addNoncePlugin());
@@ -197,11 +197,15 @@ function inlineFontsPlugin({ options }: IndexHtmlGenerator): IndexHtmlGeneratorP
   return async (html) => inlineFontsProcessor.process(html);
 }
 
-function inlineCriticalCssPlugin(generator: IndexHtmlGenerator): IndexHtmlGeneratorPlugin {
+function inlineCriticalCssPlugin(
+  generator: IndexHtmlGenerator,
+  autoCsp: boolean,
+): IndexHtmlGeneratorPlugin {
   const inlineCriticalCssProcessor = new InlineCriticalCssProcessor({
     minify: generator.options.optimization?.styles.minify,
     deployUrl: generator.options.deployUrl,
     readAsset: (filePath) => generator.readAsset(filePath),
+    autoCsp,
   });
 
   return async (html, options) =>
diff --git a/packages/angular/build/src/utils/index-file/inline-critical-css.ts b/packages/angular/build/src/utils/index-file/inline-critical-css.ts
index 47bee21456..e5106f39cf 100644
--- a/packages/angular/build/src/utils/index-file/inline-critical-css.ts
+++ b/packages/angular/build/src/utils/index-file/inline-critical-css.ts
@@ -68,6 +68,7 @@ export interface InlineCriticalCssProcessorOptions {
   minify?: boolean;
   deployUrl?: string;
   readAsset?: (path: string) => Promise<string>;
+  autoCsp?: boolean;
 }
 
 /** Partial representation of an `HTMLElement`. */
@@ -163,7 +164,7 @@ class BeastiesExtended extends BeastiesBase {
     const returnValue = await super.embedLinkedStylesheet(link, document);
     const cspNonce = this.findCspNonce(document);
 
-    if (cspNonce) {
+    if (cspNonce || this.optionsExtended.autoCsp) {
       const beastiesMedia = link.getAttribute('onload')?.match(MEDIA_SET_HANDLER_PATTERN);
 
       if (beastiesMedia) {
@@ -180,11 +181,13 @@ class BeastiesExtended extends BeastiesBase {
       // a way of doing that at the moment so we fall back to doing it any time a `link` tag is
       // inserted. We mitigate it by only iterating the direct children of the `<head>` which
       // should be pretty shallow.
-      document.head.children.forEach((child) => {
-        if (child.tagName === 'style' && !child.hasAttribute('nonce')) {
-          child.setAttribute('nonce', cspNonce);
-        }
-      });
+      if (cspNonce) {
+        document.head.children.forEach((child) => {
+          if (child.tagName === 'style' && !child.hasAttribute('nonce')) {
+            child.setAttribute('nonce', cspNonce);
+          }
+        });
+      }
     }
 
     return returnValue;
@@ -215,7 +218,7 @@ class BeastiesExtended extends BeastiesBase {
    */
   private conditionallyInsertCspLoadingScript(
     document: PartialDocument,
-    nonce: string,
+    nonce: string | null,
     link: PartialHTMLElement,
   ): void {
     if (this.addedCspScriptsDocuments.has(document)) {
@@ -223,8 +226,11 @@ class BeastiesExtended extends BeastiesBase {
     }
 
     const script = document.createElement('script');
-    script.setAttribute('nonce', nonce);
     script.textContent = LINK_LOAD_SCRIPT_CONTENT;
+    if (nonce) {
+      script.setAttribute('nonce', nonce);
+    }
+
     // Prepend the script to the head since it needs to
     // run as early as possible, before the `link` tags.
     document.head.insertBefore(script, link);
diff --git a/packages/angular/build/src/utils/index-file/inline-critical-css_spec.ts b/packages/angular/build/src/utils/index-file/inline-critical-css_spec.ts
index 4c68304cd9..86e38b39f8 100644
--- a/packages/angular/build/src/utils/index-file/inline-critical-css_spec.ts
+++ b/packages/angular/build/src/utils/index-file/inline-critical-css_spec.ts
@@ -106,6 +106,26 @@ describe('InlineCriticalCssProcessor', () => {
     expect(content).toContain('<style>body{margin:0}html{color:white}</style>');
   });
 
+  it(`should process the inline 'onload' handlers if a 'autoCsp' is true`, async () => {
+    const inlineCssProcessor = new InlineCriticalCssProcessor({
+      readAsset,
+      autoCsp: true,
+    });
+
+    const { content } = await inlineCssProcessor.process(getContent(''), {
+      outputPath: '/dist/',
+    });
+
+    expect(content).toContain(
+      '<link href="styles.css" rel="stylesheet" media="print" ngCspMedia="all">',
+    );
+    expect(tags.stripIndents`${content}`).toContain(tags.stripIndents`
+    <style>
+    body { margin: 0; }
+    html { color: white; }
+    </style>`);
+  });
+
   it('should process the inline `onload` handlers if a CSP nonce is specified', async () => {
     const inlineCssProcessor = new InlineCriticalCssProcessor({
       readAsset,
diff --git a/tests/legacy-cli/e2e/tests/build/auto-csp.ts b/tests/legacy-cli/e2e/tests/build/auto-csp.ts
index 1ea1aa5641..6b975dd5a3 100644
--- a/tests/legacy-cli/e2e/tests/build/auto-csp.ts
+++ b/tests/legacy-cli/e2e/tests/build/auto-csp.ts
@@ -1,6 +1,6 @@
 import assert from 'node:assert';
 import { getGlobalVariable } from '../../utils/env';
-import { expectFileToMatch, writeMultipleFiles } from '../../utils/fs';
+import { expectFileToMatch, writeFile, writeMultipleFiles } from '../../utils/fs';
 import { findFreePort } from '../../utils/network';
 import { execAndWaitForOutputToMatch, ng } from '../../utils/process';
 import { updateJsonFile } from '../../utils/project';
@@ -13,6 +13,9 @@ export default async function () {
     'This test should not be called in the Webpack suite.',
   );
 
+  // Add global css to trigger critical css inlining
+  await writeFile('src/styles.css', `body { color: green }`);
+
   // Turn on auto-CSP
   await updateJsonFile('angular.json', (json) => {
     const build = json['projects']['test-project']['architect']['build'];
@@ -54,7 +57,7 @@ export default async function () {
       </head>
       <body>
         <app-root></app-root>
-        
+
         <script>
           const inlineScriptBodyCreated = 1338;
           console.warn("Inline Script Body: " + inlineScriptHeadCreated);
@@ -130,6 +133,9 @@ export default async function () {
   // Make sure the output files have auto-CSP as a result of `ng build`
   await expectFileToMatch('dist/test-project/browser/index.html', CSP_META_TAG);
 
+  // Make sure if contains the critical CSS inlining CSP code.
+  await expectFileToMatch('dist/test-project/browser/index.html', 'ngCspMedia');
+
   // Make sure that our e2e protractor tests run to confirm that our angular project runs.
   const port = await spawnServer();
   await ng('e2e', `--base-url=http://localhost:${port}`, '--dev-server-target=');