diff --git a/app/assets/javascripts/bootstrap-json/index.js b/app/assets/javascripts/bootstrap-json/index.js
index bc27cac3739..6bc34b291e8 100644
--- a/app/assets/javascripts/bootstrap-json/index.js
+++ b/app/assets/javascripts/bootstrap-json/index.js
@@ -10,8 +10,11 @@ const { env } = require("node:process");
 const { glob } = require("glob");
 const { HTMLRewriter } = require("html-rewriter-wasm");
 
-async function listDistAssets() {
-  const files = await glob("**/*.js", { nodir: true, cwd: "dist/assets" });
+async function listDistAssets(outputPath) {
+  const files = await glob("**/*.js", {
+    nodir: true,
+    cwd: `${outputPath}/assets`,
+  });
   return new Set(files);
 }
 
@@ -89,7 +92,7 @@ function updateScriptReferences({
   });
 }
 
-async function handleRequest(proxy, baseURL, req, res) {
+async function handleRequest(proxy, baseURL, req, res, outputPath) {
   // x-forwarded-host is used in e.g. GitHub CodeSpaces
   let originalHost = req.headers["x-forwarded-host"] || req.headers.host;
 
@@ -178,8 +181,8 @@ async function handleRequest(proxy, baseURL, req, res) {
   if (isHTML) {
     const [responseText, chunkInfoText, distAssets] = await Promise.all([
       response.text(),
-      fsPromises.readFile("dist/assets.json", "utf-8"),
-      listDistAssets(),
+      fsPromises.readFile(`${outputPath}/assets.json`, "utf-8"),
+      listDistAssets(outputPath),
     ]);
 
     const chunkInfos = JSON.parse(chunkInfoText);
@@ -233,6 +236,7 @@ module.exports = {
   serverMiddleware(config) {
     const app = config.app;
     let { proxy, rootURL, baseURL } = config.options;
+    const outputPath = config.options.path ?? config.options.outputPath;
 
     if (!proxy) {
       // eslint-disable-next-line no-console
@@ -268,7 +272,7 @@ to serve API requests. For example:
     app.use(pathRestrictedRawMiddleware, async (req, res, next) => {
       try {
         if (this.shouldHandleRequest(req, baseURL)) {
-          await handleRequest(proxy, baseURL, req, res);
+          await handleRequest(proxy, baseURL, req, res, outputPath);
         } else {
           // Fixes issues when using e.g. "localhost" instead of loopback IP address
           req.headers.host = "127.0.0.1";