diff --git a/packages/compat/src/compat-app-builder.ts b/packages/compat/src/compat-app-builder.ts
index 32de08e87..3cf10a4c3 100644
--- a/packages/compat/src/compat-app-builder.ts
+++ b/packages/compat/src/compat-app-builder.ts
@@ -29,7 +29,6 @@ import { activePackageRules } from './dependency-rules';
 import flatMap from 'lodash/flatMap';
 import mergeWith from 'lodash/mergeWith';
 import cloneDeep from 'lodash/cloneDeep';
-import { sync as resolveSync } from 'resolve';
 import bind from 'bind-decorator';
 import { outputJSONSync, readJSONSync, rmSync, statSync, unlinkSync, writeFileSync, realpathSync } from 'fs-extra';
 import type { Options as EtcOptions } from 'babel-plugin-ember-template-compilation';
@@ -86,15 +85,6 @@ export class CompatAppBuilder {
   private extractAssets(treePaths: OutputPaths<TreeNames>): Asset[] {
     let assets: Asset[] = [];
 
-    // ember-cli traditionally outputs a dummy testem.js file to prevent
-    // spurious errors when running tests under "ember s".
-    if (this.compatApp.shouldBuildTests) {
-      let testemAsset = this.findTestemAsset();
-      if (testemAsset) {
-        assets.push(testemAsset);
-      }
-    }
-
     for (let asset of this.emberEntrypoints(treePaths.htmlTree)) {
       assets.push(asset);
     }
@@ -102,24 +92,6 @@ export class CompatAppBuilder {
     return assets;
   }
 
-  @Memoize()
-  private findTestemAsset(): Asset | undefined {
-    let sourcePath;
-    try {
-      sourcePath = resolveSync('ember-cli/lib/broccoli/testem.js', { basedir: this.root });
-    } catch (err) {}
-    if (sourcePath) {
-      let stat = statSync(sourcePath);
-      return {
-        kind: 'on-disk',
-        relativePath: 'testem.js',
-        sourcePath,
-        mtime: stat.mtime.getTime(),
-        size: stat.size,
-      };
-    }
-  }
-
   private activeAddonChildren(pkg: Package): AddonPackage[] {
     let result = (pkg.dependencies.filter(this.isActiveAddon) as AddonPackage[]).filter(
       // When looking for child addons, we want to ignore 'peerDependencies' of
diff --git a/packages/compat/src/compat-app.ts b/packages/compat/src/compat-app.ts
index 499f6c8e7..d2226e91f 100644
--- a/packages/compat/src/compat-app.ts
+++ b/packages/compat/src/compat-app.ts
@@ -14,7 +14,7 @@ import ContentForConfig from './content-for-config';
 import { V1Config, WriteV1Config } from './v1-config';
 import { WriteV1AppBoot, ReadV1AppBoot } from './v1-appboot';
 import type { AddonMeta, EmberAppInstance, OutputFileToInputFileMap, PackageInfo } from '@embroider/core';
-import { writeJSONSync, ensureDirSync, copySync, pathExistsSync, existsSync } from 'fs-extra';
+import { writeJSONSync, ensureDirSync, copySync, pathExistsSync, existsSync, writeFileSync } from 'fs-extra';
 import AddToTree from './add-to-tree';
 import DummyPackage from './dummy-package';
 import type { TransformOptions } from '@babel/core';
@@ -454,6 +454,32 @@ export default class CompatApp {
         copySync(sourcePath, destPath);
       }
 
+      if (this.shouldBuildTests) {
+        writeFileSync(
+          join(outputPath, 'testem.js'),
+          `/*
+ * This is dummy file that exists for the sole purpose
+ * of allowing tests to run directly in the browser as
+ * well as by Testem.
+ *
+ * Testem is configured to run tests directly against
+ * the test build of index.html, which requires a
+ * snippet to load the testem.js file:
+ *   <script src="/testem.js"></script>
+ * This has to go before the qunit framework and app
+ * tests are loaded.
+ *
+ * Testem internally supplies this file. However, if you
+ * run the tests directly in the browser (localhost:8000/tests),
+ * this file does not exist.
+ *
+ * Hence the purpose of this fake file. This file is served
+ * directly from the express server to satisify the script load.
+*/`
+        );
+        this._publicAssets['/testem.js'] = './testem.js';
+      }
+
       let remapAsset = this.remapAsset.bind(this);
 
       let addonMeta: AddonMeta = {