diff --git a/packages/ui/src/App.tsx b/packages/ui/src/App.tsx
index 8412a882..23ebf108 100644
--- a/packages/ui/src/App.tsx
+++ b/packages/ui/src/App.tsx
@@ -18,6 +18,7 @@ import { useRouter } from '@/hooks/useRouter';
 import { usePushVisibilityBeacon } from '@/hooks/usePushVisibilityBeacon';
 import { usePwaManifestSync } from '@/hooks/usePwaManifestSync';
 import { usePwaInstallPrompt } from '@/hooks/usePwaInstallPrompt';
+import { useWindowControlsOverlayLayout } from '@/hooks/useWindowControlsOverlayLayout';
 import { useWindowTitle } from '@/hooks/useWindowTitle';
 import { useConfigStore } from '@/stores/useConfigStore';
 import { hasModifier } from '@/lib/utils';
@@ -167,6 +168,7 @@ function SyncAppEffects({ embeddedBackgroundWorkEnabled }: {
   embeddedBackgroundWorkEnabled: boolean;
 }) {
   usePwaManifestSync();
+  useWindowControlsOverlayLayout();
   useSessionAutoCleanup(embeddedBackgroundWorkEnabled);
   useQueuedMessageAutoSend(embeddedBackgroundWorkEnabled);
   useKeyboardShortcuts();
diff --git a/packages/ui/src/components/layout/Header.tsx b/packages/ui/src/components/layout/Header.tsx
index 183dc34e..40b16e53 100644
--- a/packages/ui/src/components/layout/Header.tsx
+++ b/packages/ui/src/components/layout/Header.tsx
@@ -1356,6 +1356,19 @@ export const Header: React.FC<HeaderProps> = ({
     return '';
   }, [isDesktopApp, isMacPlatform, macosMajorVersion]);
 
+  const webWindowControlsOverlayStyle = React.useMemo<React.CSSProperties | undefined>(() => {
+    if (isDesktopApp || isVSCode) {
+      return undefined;
+    }
+
+    return {
+      paddingLeft: 'calc(0.75rem + var(--oc-wco-left-inset, 0px))',
+      paddingRight: 'calc(0.75rem + var(--oc-wco-right-inset, 0px))',
+      minHeight: 'max(3rem, var(--oc-wco-titlebar-height, 0px))',
+      height: 'max(3rem, var(--oc-wco-titlebar-height, 0px))',
+    };
+  }, [isDesktopApp, isVSCode]);
+
   const updateHeaderHeight = React.useCallback(() => {
     if (typeof document === 'undefined') {
       return;
@@ -1694,6 +1707,7 @@ export const Header: React.FC<HeaderProps> = ({
         desktopPaddingClass,
         macosHeaderSizeClass
       )}
+      style={webWindowControlsOverlayStyle}
       role="tablist"
       aria-label="Main navigation"
     >
diff --git a/packages/ui/src/components/layout/RightSidebar.tsx b/packages/ui/src/components/layout/RightSidebar.tsx
index 3780c6fe..2ecb4ba5 100644
--- a/packages/ui/src/components/layout/RightSidebar.tsx
+++ b/packages/ui/src/components/layout/RightSidebar.tsx
@@ -1,7 +1,7 @@
 import React from 'react';
 import { cn } from '@/lib/utils';
 import { useUIStore } from '@/stores/useUIStore';
-import { isDesktopShell, startDesktopWindowDrag } from '@/lib/desktop';
+import { isDesktopShell, isVSCodeRuntime, startDesktopWindowDrag } from '@/lib/desktop';
 
 export const RIGHT_SIDEBAR_CONTENT_WIDTH = 420;
 const RIGHT_SIDEBAR_MIN_WIDTH = 400;
@@ -18,6 +18,7 @@ export const RightSidebar: React.FC<RightSidebarProps> = ({ isOpen, children, cl
   const rightSidebarWidth = useUIStore((state) => state.rightSidebarWidth);
   const setRightSidebarWidth = useUIStore((state) => state.setRightSidebarWidth);
   const isDesktopApp = React.useMemo(() => isDesktopShell(), []);
+  const isVSCode = React.useMemo(() => isVSCodeRuntime(), []);
   const [isResizing, setIsResizing] = React.useState(false);
   const startXRef = React.useRef(0);
   const startWidthRef = React.useRef(rightSidebarWidth || 420);
@@ -126,6 +127,17 @@ export const RightSidebar: React.FC<RightSidebarProps> = ({ isOpen, children, cl
     await startDesktopWindowDrag();
   }, [isDesktopApp]);
 
+  const webWindowControlsOverlayStyle = React.useMemo<React.CSSProperties | undefined>(() => {
+    if (isDesktopApp || isVSCode) {
+      return undefined;
+    }
+
+    return {
+      paddingLeft: 'calc(0.75rem + var(--oc-wco-left-inset, 0px))',
+      paddingRight: 'calc(0.75rem + var(--oc-wco-right-inset, 0px))',
+    };
+  }, [isDesktopApp, isVSCode]);
+
   return (
     <aside
       ref={sidebarRef}
@@ -149,6 +161,7 @@ export const RightSidebar: React.FC<RightSidebarProps> = ({ isOpen, children, cl
         <div
           onMouseDown={handleDragStart}
           className="app-region-drag absolute inset-x-0 top-0 z-20 flex h-[var(--oc-header-height,56px)] items-center justify-end px-3"
+          style={webWindowControlsOverlayStyle}
           aria-hidden
         >
           <div
diff --git a/packages/ui/src/hooks/useWindowControlsOverlayLayout.ts b/packages/ui/src/hooks/useWindowControlsOverlayLayout.ts
new file mode 100644
index 00000000..ec6a4425
--- /dev/null
+++ b/packages/ui/src/hooks/useWindowControlsOverlayLayout.ts
@@ -0,0 +1,105 @@
+import React from 'react';
+import { isWebRuntime } from '@/lib/desktop';
+
+type WindowControlsOverlayArea = {
+  x: number;
+  width: number;
+  height: number;
+};
+
+type WindowControlsOverlayLike = {
+  visible: boolean;
+  getTitlebarAreaRect: () => WindowControlsOverlayArea;
+  addEventListener?: (type: 'geometrychange', listener: () => void) => void;
+  removeEventListener?: (type: 'geometrychange', listener: () => void) => void;
+};
+
+type NavigatorWithWindowControlsOverlay = Navigator & {
+  windowControlsOverlay?: WindowControlsOverlayLike;
+};
+
+const clampPx = (value: number): string => {
+  if (!Number.isFinite(value)) {
+    return '0px';
+  }
+  return `${Math.max(0, Math.round(value))}px`;
+};
+
+const applyOverlayInsets = (
+  root: HTMLElement,
+  leftInsetPx: number,
+  rightInsetPx: number,
+  titlebarHeightPx: number,
+) => {
+  root.style.setProperty('--oc-wco-left-inset', clampPx(leftInsetPx));
+  root.style.setProperty('--oc-wco-right-inset', clampPx(rightInsetPx));
+  root.style.setProperty('--oc-wco-titlebar-height', clampPx(titlebarHeightPx));
+};
+
+export const useWindowControlsOverlayLayout = () => {
+  React.useEffect(() => {
+    if (typeof window === 'undefined' || !isWebRuntime()) {
+      return;
+    }
+
+    const root = document.documentElement;
+    const mediaQuery = typeof window.matchMedia === 'function'
+      ? window.matchMedia('(display-mode: window-controls-overlay)')
+      : null;
+    const navigatorWithOverlay = window.navigator as NavigatorWithWindowControlsOverlay;
+    const overlay = navigatorWithOverlay.windowControlsOverlay;
+
+    const updateGeometry = () => {
+      if (!overlay || !mediaQuery?.matches || !overlay.visible) {
+        applyOverlayInsets(root, 0, 0, 0);
+        return;
+      }
+
+      const rect = overlay.getTitlebarAreaRect();
+      const leftInset = Math.max(0, Number(rect.x) || 0);
+      const width = Math.max(0, Number(rect.width) || 0);
+      const titlebarHeight = Math.max(0, Number(rect.height) || 0);
+      const rightInset = Math.max(0, window.innerWidth - (leftInset + width));
+
+      applyOverlayInsets(root, leftInset, rightInset, titlebarHeight);
+    };
+
+    const handleMediaQueryChange = () => {
+      updateGeometry();
+    };
+
+    updateGeometry();
+
+    window.addEventListener('resize', updateGeometry);
+    window.addEventListener('focus', updateGeometry);
+
+    if (mediaQuery) {
+      if (typeof mediaQuery.addEventListener === 'function') {
+        mediaQuery.addEventListener('change', handleMediaQueryChange);
+      } else if (typeof mediaQuery.addListener === 'function') {
+        mediaQuery.addListener(handleMediaQueryChange);
+      }
+    }
+
+    if (overlay && typeof overlay.addEventListener === 'function') {
+      overlay.addEventListener('geometrychange', updateGeometry);
+    }
+
+    return () => {
+      window.removeEventListener('resize', updateGeometry);
+      window.removeEventListener('focus', updateGeometry);
+
+      if (mediaQuery) {
+        if (typeof mediaQuery.removeEventListener === 'function') {
+          mediaQuery.removeEventListener('change', handleMediaQueryChange);
+        } else if (typeof mediaQuery.removeListener === 'function') {
+          mediaQuery.removeListener(handleMediaQueryChange);
+        }
+      }
+
+      if (overlay && typeof overlay.removeEventListener === 'function') {
+        overlay.removeEventListener('geometrychange', updateGeometry);
+      }
+    };
+  }, []);
+};
diff --git a/packages/ui/src/styles/design-system.css b/packages/ui/src/styles/design-system.css
index e9744281..01191f52 100644
--- a/packages/ui/src/styles/design-system.css
+++ b/packages/ui/src/styles/design-system.css
@@ -11,6 +11,9 @@
     --oc-keyboard-inset: 0px;
     --oc-keyboard-avoid-offset: 0px;
     --oc-keyboard-home-indicator: 0px;
+    --oc-wco-left-inset: 0px;
+    --oc-wco-right-inset: 0px;
+    --oc-wco-titlebar-height: 0px;
     --ui-regular-font-weight: 400;
     --oc-scrollbar-thumb: oklch(0.32 0.03 50 / 0.4);
     --oc-scrollbar-thumb-hover: oklch(0.32 0.03 50 / 0.6);
diff --git a/packages/web/index.html b/packages/web/index.html
index ecac66f9..662d1203 100644
--- a/packages/web/index.html
+++ b/packages/web/index.html
@@ -200,6 +200,7 @@
           start_url: `${baseUrl}/`,
           scope: `${baseUrl}/`,
           display: 'standalone',
+          display_override: ['window-controls-overlay'],
           ...(manifestOrientation ? { orientation: manifestOrientation } : {}),
           background_color: '#151313',
           theme_color: '#edb449',
diff --git a/packages/web/server/lib/opencode/pwa-manifest-routes.js b/packages/web/server/lib/opencode/pwa-manifest-routes.js
index 5cc08e2c..69bc2135 100644
--- a/packages/web/server/lib/opencode/pwa-manifest-routes.js
+++ b/packages/web/server/lib/opencode/pwa-manifest-routes.js
@@ -222,6 +222,7 @@ export const registerPwaManifestRoute = (app, dependencies) => {
       start_url: '/',
       scope: '/',
       display: 'standalone',
+      display_override: ['window-controls-overlay'],
       background_color: '#151313',
       theme_color: '#edb449',
       ...(manifestOrientation ? { orientation: manifestOrientation } : {}),