diff --git a/lib/browser/chrome-extension.js b/lib/browser/chrome-extension.js
index c56e3f473f..8b9c263347 100644
--- a/lib/browser/chrome-extension.js
+++ b/lib/browser/chrome-extension.js
@@ -57,18 +57,25 @@ const getManifestFromPath = function (srcDirectory) {
   if (!manifestNameMap[manifest.name]) {
     const extensionId = generateExtensionIdFromName(manifest.name)
     manifestMap[extensionId] = manifestNameMap[manifest.name] = manifest
+
+    let extensionURL = url.format({
+      protocol: 'chrome-extension',
+      slashes: true,
+      hostname: extensionId,
+      pathname: manifest.devtools_page
+    })
+
+    // Chromium requires that startPage matches '([^:]+:\/\/[^/]*)\/'
+    // We also can't use the file:// protocol here since that would make Chromium
+    // treat all extension resources as being relative to root which we don't want.
+    if (!manifest.devtools_page) extensionURL += '/'
+
     Object.assign(manifest, {
       srcDirectory: srcDirectory,
       extensionId: extensionId,
-      // We can not use 'file://' directly because all resources in the extension
-      // will be treated as relative to the root in Chrome.
-      startPage: url.format({
-        protocol: 'chrome-extension',
-        slashes: true,
-        hostname: extensionId,
-        pathname: manifest.devtools_page
-      })
+      startPage: extensionURL
     })
+
     return manifest
   } else if (manifest && manifest.name) {
     console.warn(`Attempted to load extension "${manifest.name}" that has already been loaded.`)
@@ -389,7 +396,8 @@ const loadDevToolsExtensions = function (win, manifests) {
   })
 
   extensionInfoArray.forEach((extensionInfo) => {
-    win.devToolsWebContents.executeJavaScript(`Extensions.extensionServer._addExtension(${JSON.stringify(extensionInfo)})`)
+    const info = JSON.stringify(extensionInfo)
+    win.devToolsWebContents.executeJavaScript(`Extensions.extensionServer._addExtension(${info})`)
   })
 }