diff --git a/browser/components/aboutwelcome/karma.mc.config.js b/browser/components/aboutwelcome/karma.mc.config.js
index daafcb76977a..e7f8bbb83b16 100644
--- a/browser/components/aboutwelcome/karma.mc.config.js
+++ b/browser/components/aboutwelcome/karma.mc.config.js
@@ -5,6 +5,7 @@
 const path = require("path");
 const webpack = require("webpack");
 const { ResourceUriPlugin } = require("../../tools/resourceUriPlugin");
+const { MozSrcUriPlugin } = require("../../tools/mozsrcUriPlugin");
 
 const PATHS = {
   // Where is the entry point for the unit tests?
@@ -205,6 +206,9 @@ module.exports = function (config) {
             ],
           ],
         }),
+        new MozSrcUriPlugin({
+          baseDir: path.join(__dirname, "..", "..", ".."),
+        }),
         new webpack.DefinePlugin({
           "process.env.NODE_ENV": JSON.stringify("development"),
         }),
diff --git a/browser/components/asrouter/karma.mc.config.js b/browser/components/asrouter/karma.mc.config.js
index 72fae93a948b..d1a82c80db07 100644
--- a/browser/components/asrouter/karma.mc.config.js
+++ b/browser/components/asrouter/karma.mc.config.js
@@ -5,6 +5,7 @@
 const path = require("path");
 const webpack = require("webpack");
 const { ResourceUriPlugin } = require("../../tools/resourceUriPlugin");
+const { MozSrcUriPlugin } = require("../../tools/mozsrcUriPlugin");
 
 const PATHS = {
   // Where is the entry point for the unit tests?
@@ -124,6 +125,9 @@ module.exports = function (config) {
             ],
           ],
         }),
+        new MozSrcUriPlugin({
+          baseDir: path.join(__dirname, "..", "..", ".."),
+        }),
         new webpack.DefinePlugin({
           "process.env.NODE_ENV": JSON.stringify("development"),
         }),
diff --git a/browser/extensions/newtab/karma.mc.config.js b/browser/extensions/newtab/karma.mc.config.js
index ea09c74d7d32..6e41f04c9b11 100644
--- a/browser/extensions/newtab/karma.mc.config.js
+++ b/browser/extensions/newtab/karma.mc.config.js
@@ -5,6 +5,7 @@
 const path = require("path");
 const webpack = require("webpack");
 const { ResourceUriPlugin } = require("../../tools/resourceUriPlugin");
+const { MozSrcUriPlugin } = require("../../tools/mozsrcUriPlugin");
 
 const PATHS = {
   // Where is the entry point for the unit tests?
@@ -365,6 +366,10 @@ module.exports = function (config) {
             ],
           ],
         }),
+        new MozSrcUriPlugin({
+          baseDir: path.join(__dirname, "..", "..", ".."),
+        }),
+
         new webpack.DefinePlugin({
           "process.env.NODE_ENV": JSON.stringify("development"),
         }),
diff --git a/browser/extensions/newtab/webpack.system-addon.config.js b/browser/extensions/newtab/webpack.system-addon.config.js
index 3e5cb56cb881..2aebd8cad278 100644
--- a/browser/extensions/newtab/webpack.system-addon.config.js
+++ b/browser/extensions/newtab/webpack.system-addon.config.js
@@ -5,6 +5,7 @@
 const path = require("path");
 const webpack = require("webpack");
 const { ResourceUriPlugin } = require("../../tools/resourceUriPlugin");
+const { MozSrcUriPlugin } = require("../../tools/mozsrcUriPlugin");
 
 const absolute = relPath => path.join(__dirname, relPath);
 
@@ -33,6 +34,7 @@ module.exports = (env = {}) => ({
         ],
       ],
     }),
+    new MozSrcUriPlugin({ baseDir: path.join(__dirname, "..", "..", "..") }),
     new webpack.BannerPlugin(
       `THIS FILE IS AUTO-GENERATED: ${path.basename(__filename)}`
     ),
diff --git a/browser/tools/mozsrcUriPlugin.js b/browser/tools/mozsrcUriPlugin.js
new file mode 100644
index 000000000000..6ffc94587c0e
--- /dev/null
+++ b/browser/tools/mozsrcUriPlugin.js
@@ -0,0 +1,52 @@
+/* This Source Code Form is subject to the terms of the Mozilla Public
+ * License, v. 2.0. If a copy of the MPL was not distributed with this file,
+ * You can obtain one at http://mozilla.org/MPL/2.0/. */
+
+// This plugin supports finding files with particular resource:// URIs
+// and translating the uri into a relative filesytem path where the file may be
+// found when running within the Karma / Mocha test framework.
+
+/* eslint-env node */
+const path = require("path");
+
+module.exports = {
+  MozSrcUriPlugin: class MozSrcUriPlugin {
+    /**
+     * The base directory of the repository.
+     */
+    #baseDir;
+
+    /**
+     * @param {object} options
+     *  Object passed during the instantiation of MozSrcUriPlugin
+     * @param {string} options.baseDir
+     *   The base directory of the repository.
+     */
+    constructor({ baseDir }) {
+      this.#baseDir = baseDir;
+    }
+
+    apply(compiler) {
+      compiler.hooks.compilation.tap(
+        "MozSrcUriPlugin",
+        (compilation, { normalModuleFactory }) => {
+          normalModuleFactory.hooks.resolveForScheme
+            .for("moz-src")
+            .tap("MozSrcUriPlugin", resourceData => {
+              const url = new URL(resourceData.resource);
+
+              // path.join() is necessary to normalize the path on Windows.
+              // Without it, the path may contain backslashes, resulting in
+              // different build output on Windows than on Unix systems.
+              const pathname = path.join(this.#baseDir, url.pathname);
+              resourceData.path = pathname;
+              resourceData.query = url.search;
+              resourceData.fragment = url.hash;
+              resourceData.resource = pathname + url.search + url.hash;
+              return true;
+            });
+        }
+      );
+    }
+  },
+};