diff --git a/.github/CODEOWNERS b/.github/CODEOWNERS
index f62fe0e1748..607a91d45cd 100644
--- a/.github/CODEOWNERS
+++ b/.github/CODEOWNERS
@@ -605,6 +605,7 @@ playwright.config.ts @grafana/plugins-platform-frontend
 /public/app/dev.ts @grafana/frontend-ops
 /public/app/core/utils/metrics.ts @grafana/plugins-platform-frontend
 /public/app/index.ts @grafana/frontend-ops
+/public/app/initApp.ts @grafana/frontend-ops
 /public/app/AppWrapper.tsx @grafana/frontend-ops
 /public/app/partials/ @grafana/grafana-frontend-platform
 
diff --git a/packages/grafana-runtime/src/config.ts b/packages/grafana-runtime/src/config.ts
index 7031216db7c..33f325f9f42 100644
--- a/packages/grafana-runtime/src/config.ts
+++ b/packages/grafana-runtime/src/config.ts
@@ -306,11 +306,19 @@ function overrideFeatureTogglesFromUrl(config: GrafanaBootConfig) {
   });
 }
 
-const bootData = (window as any).grafanaBootData || {
-  settings: {},
-  user: {},
-  navTree: [],
-};
+let bootData = (window as any).grafanaBootData;
+
+if (!bootData) {
+  if (process.env.NODE_ENV !== 'test') {
+    console.error('window.grafanaBootData was not set by the time config was initialized');
+  }
+
+  bootData = {
+    settings: {},
+    user: {},
+    navTree: [],
+  };
+}
 
 const options = bootData.settings;
 options.bootData = bootData;
diff --git a/pkg/api/api.go b/pkg/api/api.go
index 5503e367dfe..d131d32aedb 100644
--- a/pkg/api/api.go
+++ b/pkg/api/api.go
@@ -91,7 +91,7 @@ func (hs *HTTPServer) registerRoutes() {
 		if err != nil {
 			panic(err) // ???
 		}
-		r.Get("/mtfe", index.HandleRequest)
+		r.Get("/femt", index.HandleRequest)
 
 		// Temporarily expose the full bootdata via API
 		r.Get("/bootdata", reqNoAuth, hs.GetBootdata)
diff --git a/pkg/api/dtos/index.go b/pkg/api/dtos/index.go
index 2a55017e613..7fb4722f18b 100644
--- a/pkg/api/dtos/index.go
+++ b/pkg/api/dtos/index.go
@@ -15,7 +15,7 @@ type IndexViewData struct {
 	GoogleAnalytics4Id                  string               `json:"-"`
 	GoogleAnalytics4SendManualPageViews bool                 `json:"-"`
 	GoogleTagManagerId                  string               `json:"-"`
-	NavTree                             *navtree.NavTreeRoot `json:"navtree"`
+	NavTree                             *navtree.NavTreeRoot `json:"navTree"`
 	BuildVersion                        string               `json:"-"`
 	BuildCommit                         string               `json:"-"`
 	ThemeType                           string               `json:"-"`
diff --git a/pkg/services/frontend/index.go b/pkg/services/frontend/index.go
index 4f02bbe1127..f7fdf617b35 100644
--- a/pkg/services/frontend/index.go
+++ b/pkg/services/frontend/index.go
@@ -24,9 +24,13 @@ type IndexProvider struct {
 }
 
 type IndexViewData struct {
-	CSPContent       string
-	CSPEnabled       bool
-	IsDevelopmentEnv bool
+	CSPContent           string
+	CSPReportOnlyContent string
+	CSPEnabled           bool
+	IsDevelopmentEnv     bool
+
+	Config  *setting.Cfg
+	License licensing.Licensing
 
 	AppSubUrl    string
 	BuildVersion string
@@ -49,10 +53,6 @@ var (
 )
 
 func NewIndexProvider(cfg *setting.Cfg, license licensing.Licensing) (*IndexProvider, error) {
-	assets, err := webassets.GetWebAssets(context.Background(), cfg, license)
-	if err != nil {
-		return nil, err
-	}
 	t := htmlTemplates.Lookup("index.html")
 	if t == nil {
 		return nil, fmt.Errorf("missing index template")
@@ -66,10 +66,12 @@ func NewIndexProvider(cfg *setting.Cfg, license licensing.Licensing) (*IndexProv
 			AppSubUrl:    cfg.AppSubURL, // Based on the request?
 			BuildVersion: cfg.BuildVersion,
 			BuildCommit:  cfg.BuildCommit,
-			Assets:       assets,
+			Config:       cfg,
+			License:      license,
 
-			CSPEnabled: cfg.CSPEnabled,
-			CSPContent: cfg.CSPTemplate,
+			CSPEnabled:           cfg.CSPEnabled,
+			CSPContent:           cfg.CSPTemplate,
+			CSPReportOnlyContent: cfg.CSPReportOnlyTemplate,
 
 			IsDevelopmentEnv: cfg.Env == setting.Dev,
 		},
@@ -95,8 +97,23 @@ func (p *IndexProvider) HandleRequest(writer http.ResponseWriter, request *http.
 
 	if data.CSPEnabled {
 		data.CSPContent = middleware.ReplacePolicyVariables(p.data.CSPContent, p.data.AppSubUrl, data.Nonce)
+		writer.Header().Set("Content-Security-Policy", data.CSPContent)
+
+		policy := middleware.ReplacePolicyVariables(p.data.CSPReportOnlyContent, p.data.AppSubUrl, data.Nonce)
+		writer.Header().Set("Content-Security-Policy-Report-Only", policy)
 	}
 
+	// TODO: moved to request handler to prevent stale assets during dev,
+	// but should we do this differently?
+	assets, err := webassets.GetWebAssets(context.Background(), data.Config, data.License)
+	if err != nil {
+		p.log.Error("error getting assets", "err", err)
+		writer.WriteHeader(500)
+		return
+	}
+
+	data.Assets = assets
+
 	writer.Header().Set("Content-Type", "text/html; charset=UTF-8")
 	writer.WriteHeader(200)
 	if err := p.index.Execute(writer, &data); err != nil {
diff --git a/pkg/services/frontend/index.html b/pkg/services/frontend/index.html
index 6778c160ca7..c51574aa598 100644
--- a/pkg/services/frontend/index.html
+++ b/pkg/services/frontend/index.html
@@ -24,10 +24,83 @@
       performance.mark('frontend_boot_css_time_seconds');
     </script>
 
+    <style>
+      /*
+        Dev indicator that the page was loaded from the FEMT index.html.
+        TODO: Will remove before deploying to staging.
+      */
+      .femt-dev-frame {
+        position: fixed;
+        top: 0;
+        bottom: 1px;
+        left: 0;
+        right: 0;
+        z-index: 99999;
+        pointer-events: none;
+        border: 2px solid white;
+        border-image-source: linear-gradient(to left, #F55F3E, #FF8833);
+        border-image-slice: 1;
+      }
+    </style>
   </head>
 
   <body>
-    <h1>Grafana Frontend Server ([[.BuildVersion]])</h1>
-    <p>This is a simple static HTML page served by the Grafana frontend server module.</p>
+    <div class="femt-dev-frame"></div>
+    <div id="reactRoot"></div>
+
+    <script nonce="[[.Nonce]]">
+      [[if .Nonce]]
+        window.nonce = '[[.Nonce]]';
+      [[end]]
+
+      window.__grafana_load_failed = function(...args) {
+        console.error('Failed to load Grafana', ...args);
+      };
+
+      window.__grafana_boot_data_promise = new Promise(async (resolve) => {
+        const bootData = await fetch("/bootdata");
+
+        const rawBootData = await bootData.json();
+
+        window.grafanaBootData = {
+          _femt: true,
+          ...rawBootData,
+        }
+
+        // The per-theme CSS still contains some global styles needed
+        // to render the page correctly.
+        const cssLink = document.createElement("link");
+        cssLink.rel = 'stylesheet';
+
+        let theme = window.grafanaBootData.user.theme;
+        if (theme === "system") {
+          const darkQuery = window.matchMedia("(prefers-color-scheme: dark)");
+          theme = darkQuery.matches ? 'dark' : 'light';
+        }
+
+        if (theme === "light") {
+          document.body.classList.add("theme-light");
+          cssLink.href = window.grafanaBootData.assets.light;
+          window.grafanaBootData.user.lightTheme = true;
+        } else if (theme === "dark") {
+          document.body.classList.add("theme-dark");
+          cssLink.href = window.grafanaBootData.assets.dark;
+          window.grafanaBootData.user.lightTheme = false;
+        }
+
+        document.head.appendChild(cssLink);
+
+        resolve();
+      });
+    </script>
+
+    [[range $asset := .Assets.JSFiles]]
+      <script
+      nonce="[[$.Nonce]]"
+      src="[[$asset.FilePath]]"
+      type="text/javascript"
+      defer
+      ></script>
+    [[end]]
   </body>
 </html>
diff --git a/public/app/index.ts b/public/app/index.ts
index 7ca8aba2b14..e117cc3f598 100644
--- a/public/app/index.ts
+++ b/public/app/index.ts
@@ -1,6 +1,6 @@
-import './core/trustedTypePolicies';
-declare let __webpack_public_path__: string;
-declare let __webpack_nonce__: string;
+// The new index.html fetches window.grafanaBootData asynchronously.
+// Since much of Grafana depends on it in includes side effects at import time,
+// we delay loading the rest of the app using import() until the boot data is ready.
 
 // Check if we are hosting files on cdn and set webpack public path
 if (window.public_cdn_path) {
@@ -18,6 +18,17 @@ if (window.nonce) {
 // This is an indication to the window.onLoad failure check that the app bundle has loaded.
 window.__grafana_app_bundle_loaded = true;
 
-import app from './app';
+async function bootstrapWindowData() {
+  // Wait for window.grafanaBootData is ready. The new index.html loads it from
+  // an API call, but the old one just sets an immediately resolving promise.
+  await window.__grafana_boot_data_promise;
 
-app.init();
+  // Use eager to ensure the app is included in the initial chunk and does not
+  // require additional network requests to load.
+  await import(/* webpackMode: "eager" */ './initApp');
+}
+
+bootstrapWindowData().catch((error) => {
+  console.error('Error bootstrapping Grafana', error);
+  window.__grafana_load_failed();
+});
diff --git a/public/app/initApp.ts b/public/app/initApp.ts
new file mode 100644
index 00000000000..2f5c7fa36c5
--- /dev/null
+++ b/public/app/initApp.ts
@@ -0,0 +1,7 @@
+// See ./index.ts for why this is in a seperate file
+
+// Trusted types must be initialised before the rest of the world is imported
+import './core/trustedTypePolicies';
+import app from './app';
+
+app.init();
diff --git a/public/app/routes/routes.tsx b/public/app/routes/routes.tsx
index dc247d595f2..c79d39a2bb5 100644
--- a/public/app/routes/routes.tsx
+++ b/public/app/routes/routes.tsx
@@ -527,6 +527,11 @@ export function getAppRoutes(): RouteDescriptor[] {
         () => import(/* webpackChunkName: "BookmarksPage"*/ 'app/features/bookmarks/BookmarksPage')
       ),
     },
+    {
+      // Redirect the /femt dev page to the root
+      path: '/femt',
+      component: () => <Navigate replace to="/" />,
+    },
     ...getPluginCatalogRoutes(),
     ...getSupportBundleRoutes(),
     ...getAlertingRoutes(),
diff --git a/public/app/types/window.d.ts b/public/app/types/window.d.ts
index bf4e7c5f049..c1614d622cd 100644
--- a/public/app/types/window.d.ts
+++ b/public/app/types/window.d.ts
@@ -4,6 +4,13 @@ export declare global {
     __grafana_app_bundle_loaded: boolean;
     __grafana_public_path__: string;
     __grafana_load_failed: () => void;
+
+    /**
+     * (Potential) wait for API call to fetch boot data and place it on `window.grafanaBootData`.
+     * Required in new index.html to fetch necessary data before app init()
+     **/
+    __grafana_boot_data_promise: Promise<void>;
+
     public_cdn_path: string;
     nonce: string | undefined;
     System: typeof System;
diff --git a/public/views/index.html b/public/views/index.html
index d7c54f4967b..2ee208bbb78 100644
--- a/public/views/index.html
+++ b/public/views/index.html
@@ -275,6 +275,9 @@
         assets: [[.Assets]]
       };
 
+      // FEMT index.html uses this, and we want to keep the index.ts the same for both
+      window.__grafana_boot_data_promise = Promise.resolve();
+
       // Set theme to match system only on startup.
       // Do not react to changes in system theme after startup.
       if (window.grafanaBootData.user.theme === "system") {