diff --git a/packages/angular/build/src/tools/esbuild/angular/compiler-plugin.ts b/packages/angular/build/src/tools/esbuild/angular/compiler-plugin.ts
index f56e6c6c3119..78b395058516 100644
--- a/packages/angular/build/src/tools/esbuild/angular/compiler-plugin.ts
+++ b/packages/angular/build/src/tools/esbuild/angular/compiler-plugin.ts
@@ -29,6 +29,7 @@ import { SharedTSCompilationState, getSharedCompilationState } from './compilati
 import { ComponentStylesheetBundler } from './component-stylesheets';
 import { FileReferenceTracker } from './file-reference-tracker';
 import { setupJitPluginCallbacks } from './jit-plugin-callbacks';
+import { rewriteForBazel } from './rewrite-bazel-paths';
 import { SourceFileCache } from './source-file-cache';
 
 export interface CompilerPluginOptions {
@@ -411,8 +412,8 @@ export function createCompilerPlugin(
       });
 
       build.onLoad({ filter: /\.[cm]?[jt]sx?$/ }, async (args) => {
-        const request = path.normalize(
-          pluginOptions.fileReplacements?.[path.normalize(args.path)] ?? args.path,
+        const request = rewriteForBazel(
+          path.normalize(pluginOptions.fileReplacements?.[path.normalize(args.path)] ?? args.path),
         );
         const isJS = /\.[cm]?js$/.test(request);
 
@@ -478,13 +479,14 @@ export function createCompilerPlugin(
         return {
           contents,
           loader,
+          resolveDir: path.dirname(request),
         };
       });
 
       build.onLoad(
         { filter: /\.[cm]?js$/ },
         createCachedLoad(pluginOptions.loadResultCache, async (args) => {
-          let request = args.path;
+          let request = rewriteForBazel(args.path);
           if (pluginOptions.fileReplacements) {
             const replacement = pluginOptions.fileReplacements[path.normalize(args.path)];
             if (replacement) {
@@ -505,6 +507,7 @@ export function createCompilerPlugin(
               return {
                 contents,
                 loader: 'js',
+                resolveDir: path.dirname(request),
                 watchFiles: request !== args.path ? [request] : undefined,
               };
             },
diff --git a/packages/angular/build/src/tools/esbuild/angular/rewrite-bazel-paths.ts b/packages/angular/build/src/tools/esbuild/angular/rewrite-bazel-paths.ts
new file mode 100644
index 000000000000..8a6fb6aa82a4
--- /dev/null
+++ b/packages/angular/build/src/tools/esbuild/angular/rewrite-bazel-paths.ts
@@ -0,0 +1,30 @@
+/**
+ * @license
+ * Copyright Google LLC All Rights Reserved.
+ *
+ * Use of this source code is governed by an MIT-style license that can be
+ * found in the LICENSE file at https://angular.dev/license
+ */
+
+import { join, relative } from 'node:path';
+
+const bazelBinDirectory = process.env['BAZEL_BINDIR'];
+const bazelExecRoot = process.env['JS_BINARY__EXECROOT'];
+
+export function rewriteForBazel(path: string): string {
+  if (!bazelBinDirectory || !bazelExecRoot) {
+    return path;
+  }
+
+  const fromExecRoot = relative(bazelExecRoot, path);
+  if (!fromExecRoot.startsWith('..')) {
+    return path;
+  }
+
+  const fromBinDirectory = relative(bazelBinDirectory, path);
+  if (fromBinDirectory.startsWith('..')) {
+    return path;
+  }
+
+  return join(bazelExecRoot, fromBinDirectory);
+}