diff --git a/airflow-core/src/airflow/ui/src/components/MonacoEditor/configureMonaco.ts b/airflow-core/src/airflow/ui/src/components/MonacoEditor/configureMonaco.ts
index 629b0cc46b69c..de8b8b0ebc66c 100644
--- a/airflow-core/src/airflow/ui/src/components/MonacoEditor/configureMonaco.ts
+++ b/airflow-core/src/airflow/ui/src/components/MonacoEditor/configureMonaco.ts
@@ -25,7 +25,15 @@ type MonacoEnvironment = {
 let configurationPromise: Promise<void> | undefined;
 
 const loadMonacoModules = async () => {
-  const monacoApi = import("monaco-editor/esm/vs/editor/editor.api");
+  // `editor.api` is API-only — also load the folding contribution so `editor.foldAll` /
+  // `editor.unfoldAll` actions and the fold-gutter UI are actually registered, and the
+  // codicon styles so the gutter glyph (the `>` arrow) renders instead of an empty box.
+  // The CDN bundle used to pull these in transitively; the local ESM `editor.api` does not.
+  const monacoApi = Promise.all([
+    import("monaco-editor/esm/vs/editor/editor.api"),
+    import("monaco-editor/esm/vs/editor/contrib/folding/browser/folding"),
+    import("monaco-editor/esm/vs/base/browser/ui/codicons/codiconStyles"),
+  ]).then(([api]) => api);
 
   const workerConstructors = Promise.all([
     import("monaco-editor/esm/vs/editor/editor.worker?worker").then((module) => module.default),
diff --git a/airflow-core/src/airflow/ui/src/components/RenderedJsonField.tsx b/airflow-core/src/airflow/ui/src/components/RenderedJsonField.tsx
index ff629eaa1fb5c..76b0b2587d00c 100644
--- a/airflow-core/src/airflow/ui/src/components/RenderedJsonField.tsx
+++ b/airflow-core/src/airflow/ui/src/components/RenderedJsonField.tsx
@@ -17,7 +17,7 @@
  * under the License.
  */
 import { Flex, type FlexProps } from "@chakra-ui/react";
-import { useCallback, useState } from "react";
+import { useCallback, useEffect, useRef, useState } from "react";
 
 import Editor, { type OnMount } from "src/components/MonacoEditor";
 import { ClipboardRoot, ClipboardIconButton } from "src/components/ui";
@@ -26,6 +26,8 @@ import { useMonacoTheme } from "src/context/colorMode";
 const MAX_HEIGHT = 300;
 const MIN_HEIGHT = 40;
 
+type EditorInstance = Parameters<OnMount>[0];
+
 type Props = {
   readonly collapsed?: boolean;
   readonly content: object;
@@ -39,9 +41,12 @@ const RenderedJsonField = ({ collapsed = false, content, enableClipboard = true,
   const expandedHeight = Math.min(Math.max(lineCount * 19 + 10, MIN_HEIGHT), MAX_HEIGHT);
   const [editorHeight, setEditorHeight] = useState(collapsed ? MIN_HEIGHT : expandedHeight);
   const [isReady, setIsReady] = useState(!collapsed);
+  const editorRef = useRef<EditorInstance | null>(null);
 
   const handleMount: OnMount = useCallback(
     (editorInstance) => {
+      editorRef.current = editorInstance;
+
       editorInstance.onDidContentSizeChange(() => {
         const contentHeight = editorInstance.getContentHeight();
 
@@ -63,6 +68,21 @@ const RenderedJsonField = ({ collapsed = false, content, enableClipboard = true,
     [collapsed],
   );
 
+  // Sync fold state when the `collapsed` prop changes after mount (e.g. via Expand/Collapse All).
+  // The initial fold is handled in `handleMount` to avoid the unfolded->folded flicker.
+  useEffect(() => {
+    const editor = editorRef.current;
+
+    if (editor === null || !isReady) {
+      return;
+    }
+    const action = editor.getAction(collapsed ? "editor.foldAll" : "editor.unfoldAll");
+
+    if (action) {
+      void action.run();
+    }
+  }, [collapsed, isReady]);
+
   return (
     <Flex
       flex={1}
diff --git a/airflow-core/src/airflow/ui/src/vite-env.d.ts b/airflow-core/src/airflow/ui/src/vite-env.d.ts
index 6aefea40ce7f7..c7f6825d01418 100644
--- a/airflow-core/src/airflow/ui/src/vite-env.d.ts
+++ b/airflow-core/src/airflow/ui/src/vite-env.d.ts
@@ -24,3 +24,8 @@
 interface ImportMeta {
   readonly env: ImportMetaEnv;
 }
+
+// monaco-editor ships .d.ts only for `editor.api`; contribution side-effect imports have
+// no typings of their own.
+declare module "monaco-editor/esm/vs/editor/contrib/folding/browser/folding";
+declare module "monaco-editor/esm/vs/base/browser/ui/codicons/codiconStyles";
diff --git a/airflow-core/src/airflow/ui/vite.config.ts b/airflow-core/src/airflow/ui/vite.config.ts
index 68d62b04d82ed..a0d520269f5ef 100644
--- a/airflow-core/src/airflow/ui/vite.config.ts
+++ b/airflow-core/src/airflow/ui/vite.config.ts
@@ -39,11 +39,25 @@ export default defineConfig({
       transformIndexHtml: (html) =>
         html.replace(`src="./assets/`, `src="./static/assets/`).replace(`href="/`, `href="./`),
     },
-    cssInjectedByJsPlugin(),
+    // Keep Monaco's codicon CSS as a real CSS file (rather than inlined into JS).
+    // The codicon stylesheet references `codicon.ttf` with a CSS-relative URL — when
+    // it gets inlined into a `<style>` tag the URL resolves against the page origin
+    // (the api-server) instead of the asset directory and the font fails to load.
+    // Keeping the CSS as an emitted file lets the browser resolve the URL relative
+    // to the stylesheet's own location (`/static/assets/`). Vite still chunks it so
+    // it only loads on the routes that pull Monaco in.
+    cssInjectedByJsPlugin({
+      cssAssetsFilterFunction: (asset: { fileName: string }) => !asset.fileName.includes("codicon"),
+    }),
   ],
   resolve: { alias: { openapi: "/openapi-gen", src: "/src" } },
   server: {
     cors: true, // Only used by the dev server.
+    // The dev SPA shell is served by the airflow api-server (a different origin), so
+    // Vite must emit fully-qualified URLs — otherwise asset paths (notably worker
+    // module URLs) resolve against the api-server origin and 404. The `dev` script
+    // pins this port via --strictPort.
+    origin: "http://localhost:5173",
     proxy: {
       "/hitl-review": {
         changeOrigin: true,