diff --git a/.changeset/great-zebras-hunt.md b/.changeset/great-zebras-hunt.md
index cbb0beb1b6..252f270092 100644
--- a/.changeset/great-zebras-hunt.md
+++ b/.changeset/great-zebras-hunt.md
@@ -3,3 +3,5 @@
 ---
 
 The app build process now outputs an additional `index.html.tmpl` file. This is an non-templated version of the `index.html` file, which can be used to delay templating until runtime.
+
+The new `index.html.tmpl` file also sets a `backstage-public-path` meta tag to be templated at runtime. The meta tag is in turn picked up by the new `@backstage/cli/config/webpack-public-path.js` entry point script, which uses it to set the runtime public path of the Webpack bundle.
diff --git a/packages/cli/config/webpack-public-path.js b/packages/cli/config/webpack-public-path.js
new file mode 100644
index 0000000000..3e14e96eb9
--- /dev/null
+++ b/packages/cli/config/webpack-public-path.js
@@ -0,0 +1,31 @@
+/*
+ * Copyright 2024 The Backstage Authors
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *     http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+// This script is used to pick up and set the public path of the Webpack bundle
+// at runtime. The meta tag is injected by the app build, but only present in
+// the `index.html.tmpl` file. The runtime value of the meta tag is populated by
+// the app backend, when it templates the final `index.html` file.
+//
+// This is needed for additional chunks to use the correct public path, and it
+// is not possible to set the `__webpack_public_path__` variable outside of the
+// build itself. The Webpack output also does not read any <base> tags or
+// similar, this seems to be the only way to dynamically configure the public
+// path at runtime.
+const el = document.querySelector('meta[name="backstage-public-path"]');
+const path = el?.getAttribute('content');
+if (path) {
+  __webpack_public_path__ = path;
+}
diff --git a/packages/cli/src/lib/bundler/config.ts b/packages/cli/src/lib/bundler/config.ts
index 40ed82ef54..a64bc0fcd8 100644
--- a/packages/cli/src/lib/bundler/config.ts
+++ b/packages/cli/src/lib/bundler/config.ts
@@ -202,6 +202,8 @@ export async function createConfig(
       new HtmlWebpackPlugin({
         meta: {
           'backstage-app-mode': options?.appMode ?? 'public',
+          // This is added to be written in the later step, and finally read by the extra entry point
+          'backstage-public-path': '<%= publicPath %>/',
         },
         minify: false,
         publicPath: '<%= publicPath %>',
@@ -352,7 +354,11 @@ export async function createConfig(
     },
     devtool: isDev ? 'eval-cheap-module-source-map' : 'source-map',
     context: paths.targetPath,
-    entry: [...(options.additionalEntryPoints ?? []), paths.targetEntry],
+    entry: [
+      require.resolve('@backstage/cli/config/webpack-public-path'),
+      ...(options.additionalEntryPoints ?? []),
+      paths.targetEntry,
+    ],
     resolve: {
       extensions: ['.ts', '.tsx', '.mjs', '.js', '.jsx', '.json', '.wasm'],
       mainFields: ['browser', 'module', 'main'],