diff --git a/.prettierignore b/.prettierignore
index fff97dce442ea2..b33a5618e4d33a 100644
--- a/.prettierignore
+++ b/.prettierignore
@@ -17,6 +17,7 @@ lib/javascripts/messageformat.js
 lib/highlight_js/
 plugins/**/lib/javascripts/locale
 public/
+!/app/assets/javascripts/discourse/public
 vendor/
 app/assets/javascripts/discourse/tests/fixtures
 spec/
diff --git a/app/assets/javascripts/discourse/lib/bootstrap-json/index.js b/app/assets/javascripts/discourse/lib/bootstrap-json/index.js
index 0eb9ce0b3decec..3249cbbc6ebd7e 100644
--- a/app/assets/javascripts/discourse/lib/bootstrap-json/index.js
+++ b/app/assets/javascripts/discourse/lib/bootstrap-json/index.js
@@ -388,24 +388,30 @@ module.exports = {
 
         for (const { name, hasJs } of pluginInfos) {
           if (hasJs) {
-            scripts.push(`plugins/${name}.js`);
+            scripts.push({ src: `plugins/${name}.js`, name });
           }
 
           if (fs.existsSync(`../plugins/${name}_extras.js.erb`)) {
-            scripts.push(`plugins/${name}_extras.js`);
+            scripts.push({ src: `plugins/${name}_extras.js`, name });
           }
         }
       } else {
-        scripts.push("discourse/tests/active-plugins.js");
+        scripts.push({
+          src: "discourse/tests/active-plugins.js",
+          name: "_all",
+        });
       }
 
-      scripts.push("admin-plugins.js");
+      scripts.push({ src: "admin-plugins.js", name: "_admin" });
 
       return scripts
-        .map((s) => `<script src="${config.rootURL}assets/${s}"></script>`)
+        .map(
+          ({ src, name }) =>
+            `<script src="${config.rootURL}assets/${src}" data-discourse-plugin="${name}"></script>`
+        )
         .join("\n");
     } else if (shouldLoadPluginTestJs() && type === "test-plugin-tests-js") {
-      return `<script id="plugin-test-script" src="${config.rootURL}assets/discourse/tests/plugin-tests.js"></script>`;
+      return `<script id="plugin-test-script" src="${config.rootURL}assets/discourse/tests/plugin-tests.js" data-discourse-plugin="_all"></script>`;
     }
   },
 
diff --git a/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-listen-boot.js b/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-listen-boot.js
index 48a7c880f6b6bf..bc903572c7b33d 100644
--- a/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-listen-boot.js
+++ b/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-listen-boot.js
@@ -27,4 +27,4 @@ document.body.insertAdjacentHTML(
   `
 );
 
-require('discourse/tests/test-boot-ember-cli');
+require("discourse/tests/test-boot-ember-cli");
diff --git a/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-load-dynamic-js.js b/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-load-dynamic-js.js
new file mode 100644
index 00000000000000..fc0237c6225d3b
--- /dev/null
+++ b/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-load-dynamic-js.js
@@ -0,0 +1,28 @@
+const dynamicJsTemplate = document.querySelector("#dynamic-test-js");
+
+const params = new URLSearchParams(document.location.search);
+const skipPlugins = params.get("qunit_skip_plugins");
+
+for (const element of dynamicJsTemplate.content.childNodes) {
+  if (skipPlugins && element.dataset?.discoursePlugin) {
+    continue;
+  }
+
+  if (
+    element.tagName === "SCRIPT" &&
+    element.innerHTML.includes("EmberENV.TESTS_FILE_LOADED")
+  ) {
+    // Inline script introduced by ember-cli. Incompatible with CSP and our custom plugin JS loading system
+    // https://github.com/ember-cli/ember-cli/blob/04a38fda2c/lib/utilities/ember-app-utils.js#L131
+    // We re-implement in test-boot-ember-cli.js
+    continue;
+  }
+
+  const clone = element.cloneNode(true);
+
+  if (clone.tagName === "SCRIPT") {
+    clone.async = false;
+  }
+
+  document.querySelector("discourse-dynamic-test-js").appendChild(clone);
+}
diff --git a/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-trigger-ember-cli-boot.js b/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-trigger-ember-cli-boot.js
new file mode 100644
index 00000000000000..65f629d8a026d8
--- /dev/null
+++ b/app/assets/javascripts/discourse/public/assets/scripts/discourse-test-trigger-ember-cli-boot.js
@@ -0,0 +1 @@
+require("discourse/tests/test-boot-ember-cli");
diff --git a/app/assets/javascripts/discourse/tests/index.html b/app/assets/javascripts/discourse/tests/index.html
index e8c2e10b163351..03d82fa2db3fd1 100644
--- a/app/assets/javascripts/discourse/tests/index.html
+++ b/app/assets/javascripts/discourse/tests/index.html
@@ -50,15 +50,22 @@
     <script src="{{rootURL}}assets/discourse-markdown.js"></script>
     <script src="{{rootURL}}assets/admin.js"></script>
     <script src="{{rootURL}}assets/wizard.js"></script>
-    {{content-for "test-plugin-js"}}
-    <script src="{{rootURL}}assets/test-helpers.js"></script>
-    <script src="{{rootURL}}assets/core-tests.js"></script>
-    {{content-for "test-plugin-tests-js"}}
-    <script>
-      require("discourse/tests/test-boot-ember-cli");
-    </script>
-    <script src="{{rootURL}}assets/scripts/discourse-boot.js"></script>
 
-    {{content-for "body-footer"}} {{content-for "test-body-footer"}}
+    <template id="dynamic-test-js">
+      {{content-for "test-plugin-js"}}
+      <script defer src="{{rootURL}}assets/test-helpers.js"></script>
+      <script defer src="{{rootURL}}assets/core-tests.js"></script>
+      {{content-for "test-plugin-tests-js"}}
+      <script defer src="{{rootURL}}assets/scripts/discourse-test-trigger-ember-cli-boot.js"></script>
+      <script defer src="{{rootURL}}assets/scripts/discourse-boot.js"></script>
+      {{content-for "body-footer"}} {{content-for "test-body-footer"}}
+    </template>
+
+    <discourse-dynamic-test-js>
+    </discourse-dynamic-test-js>
+
+    <!-- This script takes the <template>, filters plugin assets as required, then appends to discourse-dynamic-test-js -->
+    <script src="{{rootURL}}assets/scripts/discourse-test-load-dynamic-js.js"></script>
+
   </body>
 </html>
diff --git a/app/assets/javascripts/discourse/tests/test-boot-ember-cli.js b/app/assets/javascripts/discourse/tests/test-boot-ember-cli.js
index c11fbcfeb57061..eabbec1ef7c85e 100644
--- a/app/assets/javascripts/discourse/tests/test-boot-ember-cli.js
+++ b/app/assets/javascripts/discourse/tests/test-boot-ember-cli.js
@@ -8,6 +8,13 @@ import { setup } from "qunit-dom";
 setEnvironment("testing");
 
 document.addEventListener("discourse-booted", () => {
+  // eslint-disable-next-line no-undef
+  if (!EmberENV.TESTS_FILE_LOADED) {
+    throw new Error(
+      'The tests file was not loaded. Make sure your tests index.html includes "assets/tests.js".'
+    );
+  }
+
   const script = document.getElementById("plugin-test-script");
   if (script && !requirejs.entries["discourse/tests/plugin-tests"]) {
     throw new Error(