diff --git a/.github/workflows/tests.yml b/.github/workflows/tests.yml
index 38e1e947c65..03d00a0f29b 100644
--- a/.github/workflows/tests.yml
+++ b/.github/workflows/tests.yml
@@ -17,7 +17,7 @@ permissions:
 
 jobs:
   build:
-    name: ${{ matrix.target }} ${{ matrix.build_type }}
+    name: ${{ matrix.target }} ${{ matrix.build_type }} ${{ ((matrix.ember_cli_plugin_assets == '1') && '(ember-cli-compiled plugin js)') || ''}}
     runs-on: ubuntu-latest
     container: discourse/discourse_test:slim${{ startsWith(matrix.build_type, 'frontend') && '-browsers' || '' }}
     timeout-minutes: 60
@@ -29,6 +29,7 @@ jobs:
       PGUSER: discourse
       PGPASSWORD: discourse
       USES_PARALLEL_DATABASES: ${{ matrix.build_type == 'backend' && matrix.target == 'core' }}
+      EMBER_CLI_PLUGIN_ASSETS: ${{ matrix.ember_cli_plugin_assets }}
 
     strategy:
       fail-fast: false
@@ -36,11 +37,17 @@ jobs:
       matrix:
         build_type: [backend, frontend, annotations]
         target: [core, plugins]
+        ember_cli_plugin_assets: ['1', '0']
         exclude:
           - build_type: annotations
             target: plugins
           - build_type: frontend
             target: core # Handled by core_frontend_tests job (below)
+          - target: core
+            ember_cli_plugin_assets: '1'
+          - target: plugins
+            build_type: backend
+            ember_cli_plugin_assets: '1'
 
     steps:
       - uses: actions/checkout@v3
diff --git a/app/assets/javascripts/discourse-hbr/raw-handlebars-compiler.js b/app/assets/javascripts/discourse-hbr/raw-handlebars-compiler.js
index f6376ca5dba..06dce159431 100644
--- a/app/assets/javascripts/discourse-hbr/raw-handlebars-compiler.js
+++ b/app/assets/javascripts/discourse-hbr/raw-handlebars-compiler.js
@@ -134,7 +134,19 @@ TemplateCompiler.prototype.initializeFeatures =
   function initializeFeatures() {};
 
 TemplateCompiler.prototype.processString = function (string, relativePath) {
-  let filename = relativePath.replace(/^templates\//, "").replace(/\.hbr$/, "");
+  let filename;
+
+  const pluginName = relativePath.match(/^discourse\/plugins\/([^\/]+)\//)?.[1];
+
+  if (pluginName) {
+    filename = relativePath
+      .replace(`discourse/plugins/${pluginName}/`, "")
+      .replace(/^(discourse\/)?templates\//, "javascripts/");
+  } else {
+    filename = relativePath.replace(/^templates\//, "");
+  }
+
+  filename = filename.replace(/\.hbr$/, "");
 
   return (
     'import { template as compiler } from "discourse-common/lib/raw-handlebars";\n' +
diff --git a/app/assets/javascripts/discourse-plugins/index.js b/app/assets/javascripts/discourse-plugins/index.js
new file mode 100644
index 00000000000..8e6742b87a1
--- /dev/null
+++ b/app/assets/javascripts/discourse-plugins/index.js
@@ -0,0 +1,120 @@
+"use strict";
+
+const path = require("path");
+const WatchedDir = require("broccoli-source").WatchedDir;
+const Funnel = require("broccoli-funnel");
+const mergeTrees = require("broccoli-merge-trees");
+const fs = require("fs");
+const concat = require("broccoli-concat");
+const RawHandlebarsCompiler = require("discourse-hbr/raw-handlebars-compiler");
+
+function fixLegacyExtensions(tree) {
+  return new Funnel(tree, {
+    getDestinationPath: function (relativePath) {
+      if (relativePath.endsWith(".es6")) {
+        return relativePath.slice(0, -4);
+      } else if (relativePath.endsWith(".raw.hbs")) {
+        return relativePath.replace(".raw.hbs", ".hbr");
+      }
+      return relativePath;
+    },
+  });
+}
+
+const COLOCATED_CONNECTOR_REGEX =
+  /^(?<prefix>.*)\/connectors\/(?<outlet>[^\/]+)\/(?<name>[^\/\.]+)\.(?<extension>.+)$/;
+
+// Having connector templates and js in the same directory causes a clash
+// when outputting es6 modules. This shim separates colocated connectors
+// into separate js / template locations.
+function unColocateConnectors(tree) {
+  return new Funnel(tree, {
+    getDestinationPath: function (relativePath) {
+      const match = relativePath.match(COLOCATED_CONNECTOR_REGEX);
+      if (
+        match &&
+        match.groups.extension === "hbs" &&
+        !match.groups.prefix.endsWith("/templates")
+      ) {
+        const { prefix, outlet, name } = match.groups;
+        return `${prefix}/templates/connectors/${outlet}/${name}.hbs`;
+      }
+      if (
+        match &&
+        match.groups.extension === "js" &&
+        match.groups.prefix.endsWith("/templates")
+      ) {
+        // Some plugins are colocating connector JS under `/templates`
+        const { prefix, outlet, name } = match.groups;
+        const newPrefix = prefix.slice(0, -"/templates".length);
+        return `${newPrefix}/connectors/${outlet}/${name}.js`;
+      }
+      return relativePath;
+    },
+  });
+}
+
+function namespaceModules(tree, pluginDirectoryName) {
+  return new Funnel(tree, {
+    getDestinationPath: function (relativePath) {
+      return `discourse/plugins/${pluginDirectoryName}/${relativePath}`;
+    },
+  });
+}
+
+module.exports = {
+  name: require("./package").name,
+
+  pluginInfos() {
+    const root = path.resolve("../../../../plugins");
+    const pluginDirectories = fs
+      .readdirSync(root, { withFileTypes: true })
+      .filter(
+        (dirent) =>
+          (dirent.isDirectory() || dirent.isSymbolicLink()) &&
+          !dirent.name.startsWith(".")
+      );
+
+    return pluginDirectories.map((directory) => {
+      const name = directory.name;
+      const jsDirectory = path.resolve(root, name, "assets/javascripts");
+      const hasJs = fs.existsSync(jsDirectory);
+      return { name, jsDirectory, hasJs };
+    });
+  },
+
+  generatePluginsTree() {
+    const trees = this.pluginInfos()
+      .filter((p) => p.hasJs)
+      .map(({ name, jsDirectory }) => {
+        let tree = new WatchedDir(jsDirectory);
+
+        tree = fixLegacyExtensions(tree);
+        tree = unColocateConnectors(tree);
+        tree = namespaceModules(tree, name);
+
+        tree = RawHandlebarsCompiler(tree);
+        tree = this.compileTemplates(tree);
+
+        tree = this.processedAddonJsFiles(tree);
+
+        return concat(mergeTrees([tree]), {
+          inputFiles: ["**/*.js"],
+          outputFile: `assets/plugins/${name}.js`,
+        });
+      });
+    return mergeTrees(trees);
+  },
+
+  shouldCompileTemplates() {
+    // The base Addon implementation checks for template
+    // files in the addon directories. We need to override that
+    // check so that the template compiler always runs.
+    return true;
+  },
+
+  treeFor() {
+    // This addon doesn't contribute any 'real' trees to the app
+    return;
+  },
+};
diff --git a/app/assets/javascripts/discourse-plugins/package.json b/app/assets/javascripts/discourse-plugins/package.json
new file mode 100644
index 00000000000..3bb0f9ed325
--- /dev/null
+++ b/app/assets/javascripts/discourse-plugins/package.json
@@ -0,0 +1,25 @@
+{
+  "name": "discourse-plugins",
+  "version": "1.0.0",
+  "description": "An addon providing a broccoli tree for each Discourse plugin",
+  "author": "Discourse",
+  "license": "GPL-2.0-only",
+  "keywords": [
+    "ember-addon"
+  ],
+  "repository": "",
+  "dependencies": {
+    "ember-auto-import": "^2.4.2",
+    "ember-cli-babel": "^7.26.10",
+    "ember-cli-htmlbars": "^6.1.0",
+    "discourse-widget-hbs": "1.0"
+  },
+  "engines": {
+    "node": "16.* || >= 18",
+    "npm": "please-use-yarn",
+    "yarn": ">= 1.21.1"
+  },
+  "ember": {
+    "edition": "default"
+  }
+}
diff --git a/app/assets/javascripts/discourse/app/lib/plugin-connectors.js b/app/assets/javascripts/discourse/app/lib/plugin-connectors.js
index abc6bc4ac6e..bcee944c053 100644
--- a/app/assets/javascripts/discourse/app/lib/plugin-connectors.js
+++ b/app/assets/javascripts/discourse/app/lib/plugin-connectors.js
@@ -45,7 +45,12 @@ function findClass(outletName, uniqueName) {
   if (!_classPaths) {
     _classPaths = {};
     findOutlets(require._eak_seen, (outlet, res, un) => {
-      _classPaths[`${outlet}/${un}`] = requirejs(res).default;
+      const possibleConnectorClass = requirejs(res).default;
+      if (possibleConnectorClass.__id) {
+        // This is the template, not the connector class
+        return;
+      }
+      _classPaths[`${outlet}/${un}`] = possibleConnectorClass;
     });
   }
 
diff --git a/app/assets/javascripts/discourse/app/lib/source-identifier.js b/app/assets/javascripts/discourse/app/lib/source-identifier.js
index 555c1cac8c0..de0fbd7e373 100644
--- a/app/assets/javascripts/discourse/app/lib/source-identifier.js
+++ b/app/assets/javascripts/discourse/app/lib/source-identifier.js
@@ -30,10 +30,10 @@ export default function identifySource(error) {
 
   let plugin;
 
-  if (isDevelopment()) {
-    // Source-mapped:
-    plugin = plugin || error.stack.match(/plugins\/([\w-]+)\//)?.[1];
+  // Source-mapped:
+  plugin = plugin || error.stack.match(/plugins\/([\w-]+)\//)?.[1];
 
+  if (isDevelopment()) {
     // Un-source-mapped:
     plugin = plugin || error.stack.match(/assets\/plugins\/([\w-]+)\.js/)?.[1];
   }
diff --git a/app/assets/javascripts/discourse/ember-cli-build.js b/app/assets/javascripts/discourse/ember-cli-build.js
index 15cc37a4ae0..f6a59caac3c 100644
--- a/app/assets/javascripts/discourse/ember-cli-build.js
+++ b/app/assets/javascripts/discourse/ember-cli-build.js
@@ -14,6 +14,7 @@ const SILENCED_WARN_PREFIXES = [
   "Setting the `jquery-integration` optional feature flag",
   "The Ember Classic edition has been deprecated",
   "Setting the `template-only-glimmer-components` optional feature flag to `false`",
+  "DEPRECATION: Invoking the `<LinkTo>` component with positional arguments is deprecated",
 ];
 
 module.exports = function (defaults) {
@@ -29,6 +30,16 @@ module.exports = function (defaults) {
     }
   };
 
+  // Silence warnings which go straight to console.warn (e.g. template compiler deprecations)
+  /* eslint-disable no-console */
+  const oldConsoleWarn = console.warn.bind(console);
+  console.warn = (message, ...args) => {
+    if (!SILENCED_WARN_PREFIXES.some((prefix) => message.startsWith(prefix))) {
+      return oldConsoleWarn(message, ...args);
+    }
+  };
+  /* eslint-enable no-console */
+
   const isProduction = EmberApp.env().includes("production");
   const isTest = EmberApp.env().includes("test");
 
@@ -134,6 +145,16 @@ module.exports = function (defaults) {
       "/app/assets/javascripts/discourse/public/assets/scripts/module-shims.js"
   );
 
+  let discoursePluginsTree;
+  if (process.env.EMBER_CLI_PLUGIN_ASSETS === "1") {
+    discoursePluginsTree = app.project
+      .findAddonByName("discourse-plugins")
+      .generatePluginsTree();
+  } else {
+    // Empty tree - no-op
+    discoursePluginsTree = mergeTrees([]);
+  }
+
   const terserPlugin = app.project.findAddonByName("ember-cli-terser");
   const applyTerser = (tree) => terserPlugin.postprocessTree("all", tree);
 
@@ -164,5 +185,6 @@ module.exports = function (defaults) {
       inputFiles: [`discourse-boot.js`],
     }),
     generateScriptsTree(app),
+    applyTerser(discoursePluginsTree),
   ]);
 };
diff --git a/app/assets/javascripts/discourse/lib/bootstrap-json/index.js b/app/assets/javascripts/discourse/lib/bootstrap-json/index.js
index 50ebf5daa97..0eb9ce0b3de 100644
--- a/app/assets/javascripts/discourse/lib/bootstrap-json/index.js
+++ b/app/assets/javascripts/discourse/lib/bootstrap-json/index.js
@@ -5,7 +5,8 @@ const fetch = require("node-fetch");
 const { encode } = require("html-entities");
 const cleanBaseURL = require("clean-base-url");
 const path = require("path");
-const { promises: fs } = require("fs");
+const fs = require("fs");
+const fsPromises = fs.promises;
 const { JSDOM } = require("jsdom");
 const { shouldLoadPluginTestJs } = require("discourse/lib/plugin-js");
 const { Buffer } = require("node:buffer");
@@ -231,7 +232,7 @@ async function applyBootstrap(bootstrap, template, response, baseURL, preload) {
 
 async function buildFromBootstrap(proxy, baseURL, req, response, preload) {
   try {
-    const template = await fs.readFile(
+    const template = await fsPromises.readFile(
       path.join(cwd(), "dist", "index.html"),
       "utf8"
     );
@@ -378,10 +379,31 @@ module.exports = {
 
   contentFor(type, config) {
     if (shouldLoadPluginTestJs() && type === "test-plugin-js") {
-      return `
-        <script src="${config.rootURL}assets/discourse/tests/active-plugins.js"></script>
-        <script src="${config.rootURL}assets/admin-plugins.js"></script>
-      `;
+      const scripts = [];
+
+      if (process.env.EMBER_CLI_PLUGIN_ASSETS === "1") {
+        const pluginInfos = this.app.project
+          .findAddonByName("discourse-plugins")
+          .pluginInfos();
+
+        for (const { name, hasJs } of pluginInfos) {
+          if (hasJs) {
+            scripts.push(`plugins/${name}.js`);
+          }
+
+          if (fs.existsSync(`../plugins/${name}_extras.js.erb`)) {
+            scripts.push(`plugins/${name}_extras.js`);
+          }
+        }
+      } else {
+        scripts.push("discourse/tests/active-plugins.js");
+      }
+
+      scripts.push("admin-plugins.js");
+
+      return scripts
+        .map((s) => `<script src="${config.rootURL}assets/${s}"></script>`)
+        .join("\n");
     } else if (shouldLoadPluginTestJs() && type === "test-plugin-tests-js") {
       return `<script id="plugin-test-script" src="${config.rootURL}assets/discourse/tests/plugin-tests.js"></script>`;
     }
diff --git a/app/assets/javascripts/discourse/package.json b/app/assets/javascripts/discourse/package.json
index 00b7b4c9fa6..ec34e659cdd 100644
--- a/app/assets/javascripts/discourse/package.json
+++ b/app/assets/javascripts/discourse/package.json
@@ -33,6 +33,7 @@
     "@uppy/utils": "^4.1.0",
     "@uppy/xhr-upload": "^2.1.2",
     "admin": "^1.0.0",
+    "discourse-plugins": "^1.0.0",
     "bootstrap": "3.4.1",
     "broccoli-asset-rev": "^3.0.0",
     "deepmerge": "^4.2.2",
diff --git a/app/assets/javascripts/discourse/public/assets/scripts/discourse-boot.js b/app/assets/javascripts/discourse/public/assets/scripts/discourse-boot.js
index 7dab11a480b..b3f56a6dcc5 100644
--- a/app/assets/javascripts/discourse/public/assets/scripts/discourse-boot.js
+++ b/app/assets/javascripts/discourse/public/assets/scripts/discourse-boot.js
@@ -4,15 +4,34 @@
   }
 
   // TODO: Remove this and have resolver find the templates
-  const prefix = "discourse/templates/";
+  const discoursePrefix = "discourse/templates/";
   const adminPrefix = "admin/templates/";
   const wizardPrefix = "wizard/templates/";
-  let len = prefix.length;
+  const discoursePrefixLength = discoursePrefix.length;
+
+  const pluginRegex = /^discourse\/plugins\/([^\/]+)\//;
+
   Object.keys(requirejs.entries).forEach(function (key) {
-    if (key.startsWith(prefix)) {
-      Ember.TEMPLATES[key.slice(len)] = require(key).default;
+    let templateKey;
+    let pluginName;
+    if (key.startsWith(discoursePrefix)) {
+      templateKey = key.slice(discoursePrefixLength);
     } else if (key.startsWith(adminPrefix) || key.startsWith(wizardPrefix)) {
-      Ember.TEMPLATES[key] = require(key).default;
+      templateKey = key;
+    } else if (
+      (pluginName = key.match(pluginRegex)?.[1]) &&
+      key.includes("/templates/") &&
+      require(key).default.__id // really is a template
+    ) {
+      // This logic mimics the old sprockets compilation system which used to
+      // output templates directly to `Ember.TEMPLATES` with this naming logic
+      templateKey = key.slice(`discourse/plugins/${pluginName}/`.length);
+      templateKey = templateKey.replace("discourse/templates/", "");
+      templateKey = `javascripts/${templateKey}`;
+    }
+
+    if (templateKey) {
+      Ember.TEMPLATES[templateKey] = require(key).default;
     }
   });
 
diff --git a/app/assets/javascripts/discourse/testem.js b/app/assets/javascripts/discourse/testem.js
index 8da35eb44e9..d49180f5c48 100644
--- a/app/assets/javascripts/discourse/testem.js
+++ b/app/assets/javascripts/discourse/testem.js
@@ -95,6 +95,9 @@ if (process.argv.includes("-t")) {
 } else if (shouldLoadPluginTestJs()) {
   // Running with ember cli, but we want to pass through plugin request to Rails
   module.exports.proxies = {
+    "/assets/plugins/*_extra.js": {
+      target,
+    },
     "/assets/discourse/tests/active-plugins.js": {
       target,
     },
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 3ada4484ab8..c11fbcfeb57 100644
--- a/app/assets/javascripts/discourse/tests/test-boot-ember-cli.js
+++ b/app/assets/javascripts/discourse/tests/test-boot-ember-cli.js
@@ -9,7 +9,7 @@ setEnvironment("testing");
 
 document.addEventListener("discourse-booted", () => {
   const script = document.getElementById("plugin-test-script");
-  if (script && !requirejs.entries["discourse/tests/active-plugins"]) {
+  if (script && !requirejs.entries["discourse/tests/plugin-tests"]) {
     throw new Error(
       `Plugin JS payload failed to load from ${script.src}. Is the Rails server running?`
     );
diff --git a/app/assets/javascripts/package.json b/app/assets/javascripts/package.json
index 43154f4212c..d5719f80010 100644
--- a/app/assets/javascripts/package.json
+++ b/app/assets/javascripts/package.json
@@ -3,6 +3,7 @@
   "workspaces": [
     "discourse",
     "admin",
+    "discourse-plugins",
     "discourse-common",
     "discourse-ensure-deprecation-order",
     "discourse-hbr",
diff --git a/app/views/qunit/theme.html.erb b/app/views/qunit/theme.html.erb
index c5e1071b5fa..c6d026d9edc 100644
--- a/app/views/qunit/theme.html.erb
+++ b/app/views/qunit/theme.html.erb
@@ -8,7 +8,9 @@
       <%= preload_script "vendor" %>
       <%= preload_script "discourse" %>
       <%= preload_script "admin" %>
-      <%= preload_script "discourse/tests/active-plugins" %>
+      <%- Discourse.find_plugin_js_assets(include_disabled: true).each do |file| %>
+        <%= preload_script file %>
+      <%- end %>
       <%= preload_script "admin-plugins" %>
       <%= preload_script "test-support" %>
       <%= preload_script "test-helpers" %>
diff --git a/config/initializers/assets.rb b/config/initializers/assets.rb
index 504a14de96c..829465d1a30 100644
--- a/config/initializers/assets.rb
+++ b/config/initializers/assets.rb
@@ -53,7 +53,7 @@ Rails.application.config.assets.precompile += %w{
   scripts/discourse-boot
 }
 
-Rails.application.config.assets.precompile += EmberCli::ASSETS.map { |name| name.sub('.js', '.map') }
+Rails.application.config.assets.precompile += EmberCli.assets.map { |name| name.sub('.js', '.map') }
 
 # Precompile all available locales
 unless GlobalSetting.try(:omit_base_locales)
diff --git a/lib/discourse.rb b/lib/discourse.rb
index 43659294fdc..526f6b8ee35 100644
--- a/lib/discourse.rb
+++ b/lib/discourse.rb
@@ -382,12 +382,17 @@ module Discourse
 
   def self.find_plugin_js_assets(args)
     plugins = self.find_plugins(args).select do |plugin|
-      plugin.js_asset_exists?
+      plugin.js_asset_exists? || plugin.extra_js_asset_exists?
     end
 
     plugins = apply_asset_filters(plugins, :js, args[:request])
 
-    plugins.map { |plugin| "plugins/#{plugin.directory_name}" }
+    plugins.flat_map do |plugin|
+      assets = []
+      assets << "plugins/#{plugin.directory_name}" if plugin.js_asset_exists?
+      assets << "plugins/#{plugin.directory_name}_extra" if plugin.extra_js_asset_exists?
+      assets
+    end
   end
 
   def self.assets_digest
diff --git a/lib/discourse_sourcemapping_url_processor.rb b/lib/discourse_sourcemapping_url_processor.rb
index 51c3ba21b2a..7b6ae82d563 100644
--- a/lib/discourse_sourcemapping_url_processor.rb
+++ b/lib/discourse_sourcemapping_url_processor.rb
@@ -6,7 +6,7 @@
 class DiscourseSourcemappingUrlProcessor < Sprockets::Rails::SourcemappingUrlProcessor
   def self.sourcemap_asset_path(sourcemap_logical_path, context:)
     result = super(sourcemap_logical_path, context: context)
-    if File.basename(sourcemap_logical_path) === sourcemap_logical_path
+    if (File.basename(sourcemap_logical_path) === sourcemap_logical_path) || sourcemap_logical_path.start_with?("plugins/")
       # If the original sourcemap reference is relative, keep it relative
       result = File.basename(result)
     end
diff --git a/lib/ember_cli.rb b/lib/ember_cli.rb
index efae6be1697..7135e96a46a 100644
--- a/lib/ember_cli.rb
+++ b/lib/ember_cli.rb
@@ -1,15 +1,33 @@
 # frozen_string_literal: true
 
 module EmberCli
-  ASSETS = %w(
-    discourse.js
-    admin.js
-    wizard.js
-    ember_jquery.js
-    pretty-text-bundle.js
-    start-discourse.js
-    vendor.js
-  ) + Dir.glob("app/assets/javascripts/discourse/scripts/*.js").map { |f| File.basename(f) }
+  def self.plugin_assets?
+    ENV["EMBER_CLI_PLUGIN_ASSETS"] == "1"
+  end
+
+  def self.assets
+    @assets ||= begin
+      assets = %w(
+        discourse.js
+        admin.js
+        wizard.js
+        ember_jquery.js
+        pretty-text-bundle.js
+        start-discourse.js
+        vendor.js
+      )
+      assets += Dir.glob("app/assets/javascripts/discourse/scripts/*.js").map { |f| File.basename(f) }
+
+      if plugin_assets?
+        Discourse.find_plugin_js_assets(include_disabled: true).each do |file|
+          next if file.ends_with?("_extra") # these are still handled by sprockets
+          assets << "#{file}.js"
+        end
+      end
+
+      assets
+    end
+  end
 
   def self.script_chunks
     return @@chunk_infos if defined? @@chunk_infos
@@ -29,6 +47,6 @@ module EmberCli
   end
 
   def self.is_ember_cli_asset?(name)
-    ASSETS.include?(name) || name.start_with?("chunk.")
+    assets.include?(name) || name.start_with?("chunk.")
   end
 end
diff --git a/lib/plugin/instance.rb b/lib/plugin/instance.rb
index 8b3eb2294f7..05d3685b296 100644
--- a/lib/plugin/instance.rb
+++ b/lib/plugin/instance.rb
@@ -715,19 +715,31 @@ class Plugin::Instance
     handlebars_includes.each { |hb| contents << "require_asset('#{hb}')" }
     javascript_includes.each { |js| contents << "require_asset('#{js}')" }
 
-    each_globbed_asset do |f, is_dir|
-      contents << (is_dir ? "depend_on('#{f}')" : "require_asset('#{f}')")
+    if !EmberCli.plugin_assets?
+      each_globbed_asset do |f, is_dir|
+        contents << (is_dir ? "depend_on('#{f}')" : "require_asset('#{f}')")
+      end
     end
 
-    if contents.present?
-      contents.insert(0, "<%")
-      contents << "%>"
-      Discourse::Utils.atomic_write_file(js_file_path, contents.join("\n"))
-    else
-      begin
-        File.delete(js_file_path)
+    if !contents.present?
+      [js_file_path, extra_js_file_path].each do |f|
+        File.delete(f)
       rescue Errno::ENOENT
       end
+      return
+    end
+
+    contents.insert(0, "<%")
+    contents << "%>"
+
+    write_path = EmberCli.plugin_assets? ? extra_js_file_path : js_file_path
+    delete_path = EmberCli.plugin_assets? ? js_file_path : extra_js_file_path
+
+    Discourse::Utils.atomic_write_file(write_path, contents.join("\n"))
+
+    begin
+      File.delete(delete_path)
+    rescue Errno::ENOENT
     end
   end
 
@@ -838,7 +850,16 @@ class Plugin::Instance
   end
 
   def js_asset_exists?
-    File.exist?(js_file_path)
+    if EmberCli.plugin_assets?
+      # If assets/javascripts exists, ember-cli will output a .js file
+      File.exist?("#{File.dirname(@path)}/assets/javascripts")
+    else
+      File.exist?(js_file_path)
+    end
+  end
+
+  def extra_js_asset_exists?
+    EmberCli.plugin_assets? && File.exist?(extra_js_file_path)
   end
 
   # Receives an array with two elements:
@@ -1080,7 +1101,11 @@ class Plugin::Instance
   end
 
   def js_file_path
-    @file_path ||= "#{Plugin::Instance.js_path}/#{directory_name}.js.erb"
+    "#{Plugin::Instance.js_path}/#{directory_name}.js.erb"
+  end
+
+  def extra_js_file_path
+    @extra_js_file_path ||= "#{Plugin::Instance.js_path}/#{directory_name}_extra.js.erb"
   end
 
   def register_assets!