diff --git a/app/src/components/MeshGradient.test.tsx b/app/src/components/MeshGradient.test.tsx
index 4d48408dc..0956f4ab7 100644
--- a/app/src/components/MeshGradient.test.tsx
+++ b/app/src/components/MeshGradient.test.tsx
@@ -1,24 +1,45 @@
 import { act } from '@testing-library/react';
-import { beforeEach, describe, expect, it, vi } from 'vitest';
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest';
 
 import ThemeProvider from '../providers/ThemeProvider';
 import { setThemeToken, upsertCustomTheme } from '../store/themeSlice';
 import { renderWithProviders } from '../test/test-utils';
 import MeshGradient from './MeshGradient';
 
-const gradientMock = vi.hoisted(() => ({
-  disconnect: vi.fn(),
-  // eslint-disable-next-line prefer-arrow-callback -- constructor mock must be new-able; arrows are not constructible.
-  Gradient: vi.fn(function MockGradient() {
-    return {
-      disconnect: gradientMock.disconnect,
-      initGradient: gradientMock.initGradient,
-      pause: gradientMock.pause,
-    };
-  }),
-  initGradient: vi.fn(),
-  pause: vi.fn(),
-}));
+const gradientMock = vi.hoisted(() => {
+  // Shared play flag, mirroring the real `Gradient.conf.playing`, so the
+  // component's double-schedule guard (`shouldAnimate === playing`) is exercised.
+  const conf = { playing: false };
+  // `state.mesh` mirrors `Gradient.mesh`: truthy once a WebGL context is
+  // acquired, `undefined` on no-GPU/headless. The component only calls play()
+  // when it is set (#3524); a getter lets a test flip it before events fire.
+  const state: { mesh: unknown } = { mesh: {} };
+  return {
+    conf,
+    state,
+    disconnect: vi.fn(),
+    initGradient: vi.fn(),
+    pause: vi.fn(() => {
+      conf.playing = false;
+    }),
+    play: vi.fn(() => {
+      conf.playing = true;
+    }),
+    // eslint-disable-next-line prefer-arrow-callback -- constructor mock must be new-able; arrows are not constructible.
+    Gradient: vi.fn(function MockGradient() {
+      return {
+        conf,
+        get mesh() {
+          return state.mesh;
+        },
+        disconnect: gradientMock.disconnect,
+        initGradient: gradientMock.initGradient,
+        pause: gradientMock.pause,
+        play: gradientMock.play,
+      };
+    }),
+  };
+});
 
 vi.mock('../lib/meshGradient', () => ({ Gradient: gradientMock.Gradient }));
 
@@ -30,6 +51,12 @@ describe('<MeshGradient />', () => {
     gradientMock.Gradient.mockClear();
     gradientMock.initGradient.mockClear();
     gradientMock.pause.mockClear();
+    gradientMock.play.mockClear();
+    gradientMock.conf.playing = false;
+    gradientMock.state.mesh = {}; // default: WebGL mesh initialized OK
+    // Default to a visible, focused window so the gradient animates unless a
+    // test says otherwise.
+    vi.spyOn(document, 'hasFocus').mockReturnValue(true);
     rafQueue = [];
     vi.spyOn(window, 'requestAnimationFrame').mockImplementation(callback => {
       rafQueue.push(callback);
@@ -38,6 +65,10 @@ describe('<MeshGradient />', () => {
     vi.spyOn(window, 'cancelAnimationFrame').mockImplementation(() => {});
   });
 
+  afterEach(() => {
+    vi.restoreAllMocks();
+  });
+
   function flushAnimationFrames() {
     const pending = [...rafQueue];
     rafQueue = [];
@@ -90,4 +121,70 @@ describe('<MeshGradient />', () => {
     expect(gradientMock.pause).toHaveBeenCalledTimes(1);
     expect(gradientMock.initGradient).toHaveBeenCalledTimes(2);
   });
+
+  it('pauses the animation when the window loses focus and resumes when it returns (#3524)', () => {
+    const hasFocus = vi.spyOn(document, 'hasFocus').mockReturnValue(true);
+
+    renderWithProviders(
+      <ThemeProvider>
+        <MeshGradient />
+      </ThemeProvider>
+    );
+    act(() => {
+      flushAnimationFrames();
+    });
+
+    // Focused + visible on mount → animating.
+    expect(gradientMock.play).toHaveBeenCalledTimes(1);
+    expect(gradientMock.conf.playing).toBe(true);
+    gradientMock.play.mockClear();
+    gradientMock.pause.mockClear();
+
+    // Window backgrounded (occluded/blurred) → the shader must stop rendering.
+    hasFocus.mockReturnValue(false);
+    act(() => {
+      window.dispatchEvent(new Event('blur'));
+    });
+    expect(gradientMock.pause).toHaveBeenCalledTimes(1);
+    expect(gradientMock.conf.playing).toBe(false);
+
+    // Window refocused → resume.
+    hasFocus.mockReturnValue(true);
+    act(() => {
+      window.dispatchEvent(new Event('focus'));
+    });
+    expect(gradientMock.play).toHaveBeenCalledTimes(1);
+    expect(gradientMock.conf.playing).toBe(true);
+  });
+
+  it('never resumes when the WebGL mesh failed to initialize (no-GPU/Tauri, #3524)', () => {
+    // Simulate a gradient whose connect() couldn't get a GL context: no `mesh`
+    // was ever built, yet the real lib leaves `conf.playing` truthy. play() must
+    // stay suppressed so the animation loop never dereferences the missing mesh.
+    gradientMock.state.mesh = undefined;
+    gradientMock.conf.playing = true;
+
+    const hasFocus = vi.spyOn(document, 'hasFocus').mockReturnValue(true);
+    renderWithProviders(
+      <ThemeProvider>
+        <MeshGradient />
+      </ThemeProvider>
+    );
+    act(() => {
+      flushAnimationFrames();
+    });
+
+    // Blur then refocus — the resume path must NOT call play() without a mesh
+    // (previously this crashed on the next animation frame).
+    hasFocus.mockReturnValue(false);
+    act(() => {
+      window.dispatchEvent(new Event('blur'));
+    });
+    hasFocus.mockReturnValue(true);
+    act(() => {
+      window.dispatchEvent(new Event('focus'));
+    });
+
+    expect(gradientMock.play).not.toHaveBeenCalled();
+  });
 });
diff --git a/app/src/components/MeshGradient.tsx b/app/src/components/MeshGradient.tsx
index d52358f5c..cac150ec1 100644
--- a/app/src/components/MeshGradient.tsx
+++ b/app/src/components/MeshGradient.tsx
@@ -47,6 +47,40 @@ export default function MeshGradient() {
       }
     };
 
+    // Only animate when the app window is actually visible AND focused, and the
+    // user hasn't asked for reduced motion. A full-screen WebGL shader that keeps
+    // rendering every frame while the app merely sits open in the background
+    // (occluded/blurred) or minimized is pure wasted GPU/CPU — the sustained
+    // load users see as the machine running hot with nothing happening (#3524).
+    const prefersReducedMotion = () =>
+      typeof window !== 'undefined' && typeof window.matchMedia === 'function'
+        ? window.matchMedia('(prefers-reduced-motion: reduce)').matches
+        : false;
+
+    const applyPlayState = () => {
+      if (!gradient) return;
+      const shouldAnimate = !document.hidden && document.hasFocus() && !prefersReducedMotion();
+      // Read the gradient's own play flag so we never double-schedule its rAF
+      // loop (calling play() while already playing starts a second loop).
+      const playing = gradient.conf?.playing ?? false;
+      if (shouldAnimate === playing) return;
+      try {
+        // Only (re)start once the WebGL mesh actually initialized. On a no-GPU /
+        // headless environment `connect()` leaves `conf.playing` truthy without
+        // ever creating `mesh`, so resuming here would schedule `animate`, which
+        // dereferences `mesh.material` on the next frame and throws — exactly the
+        // environment this component is meant to tolerate (#3524). `pause()` is
+        // always safe (it just clears the flag / cancels any rAF).
+        if (shouldAnimate) {
+          if (gradient.mesh) gradient.play();
+        } else {
+          gradient.pause();
+        }
+      } catch {
+        // Play-state control is best-effort.
+      }
+    };
+
     const start = () => {
       if (disposed) return;
       const root = document.documentElement;
@@ -67,6 +101,9 @@ export default function MeshGradient() {
       try {
         gradient = new Gradient();
         gradient.initGradient('#mesh-gradient');
+        // Honor the current visibility/focus/reduced-motion state right away, so
+        // a gradient created while the window is backgrounded never animates.
+        applyPlayState();
       } catch (err) {
         console.warn('[MeshGradient] WebGL init failed, gradient disabled:', err);
         gradient = null;
@@ -82,6 +119,25 @@ export default function MeshGradient() {
 
     scheduleStart();
 
+    // Pause/resume the animation as the window gains or loses visibility/focus
+    // (and when the reduced-motion preference flips), so it only ever burns
+    // cycles while the user is actually looking at a focused OpenHuman window.
+    const onPlayStateChange = () => applyPlayState();
+    document.addEventListener('visibilitychange', onPlayStateChange);
+    window.addEventListener('focus', onPlayStateChange);
+    window.addEventListener('blur', onPlayStateChange);
+    let removeMotionListener: (() => void) | undefined;
+    if (typeof window !== 'undefined' && window.matchMedia) {
+      const motionMq = window.matchMedia('(prefers-reduced-motion: reduce)');
+      if (motionMq.addEventListener) {
+        motionMq.addEventListener('change', onPlayStateChange);
+        removeMotionListener = () => motionMq.removeEventListener('change', onPlayStateChange);
+      } else {
+        motionMq.addListener(onPlayStateChange);
+        removeMotionListener = () => motionMq.removeListener(onPlayStateChange);
+      }
+    }
+
     let removeSystemListener: (() => void) | undefined;
     if (variant === 'system' && typeof window !== 'undefined' && window.matchMedia) {
       const mq = window.matchMedia('(prefers-color-scheme: dark)');
@@ -98,6 +154,10 @@ export default function MeshGradient() {
     return () => {
       disposed = true;
       removeSystemListener?.();
+      removeMotionListener?.();
+      document.removeEventListener('visibilitychange', onPlayStateChange);
+      window.removeEventListener('focus', onPlayStateChange);
+      window.removeEventListener('blur', onPlayStateChange);
       window.cancelAnimationFrame(raf);
       disconnectGradient();
     };
diff --git a/app/src/lib/meshGradient.d.ts b/app/src/lib/meshGradient.d.ts
index c53c0b70f..6b6621fb1 100644
--- a/app/src/lib/meshGradient.d.ts
+++ b/app/src/lib/meshGradient.d.ts
@@ -5,6 +5,13 @@ export interface GradientConfig {
 export class Gradient {
   el?: HTMLCanvasElement;
   conf?: GradientConfig;
+  /**
+   * The WebGL mesh. Only set once `connect()` acquires a GL context and builds
+   * the geometry; stays `undefined` on no-GPU / headless environments. Callers
+   * must check it before `play()`, since the animation loop dereferences
+   * `mesh.material` and would throw when it is absent (#3524).
+   */
+  mesh?: unknown;
   play(): void;
   pause(): void;
   disconnect(): void;