diff --git a/dom/canvas/OffscreenCanvas.cpp b/dom/canvas/OffscreenCanvas.cpp
index 4b8a3816cadb..b5fe51f411e2 100644
--- a/dom/canvas/OffscreenCanvas.cpp
+++ b/dom/canvas/OffscreenCanvas.cpp
@@ -48,7 +48,6 @@ OffscreenCanvas::OffscreenCanvas(nsIGlobalObject* aGlobal, uint32_t aWidth,
                                  layers::TextureType aTextureType,
                                  OffscreenCanvasDisplayHelper* aDisplay)
     : DOMEventTargetHelper(aGlobal),
-      mAttrDirty(false),
       mNeutered(false),
       mIsWriteOnly(false),
       mWidth(aWidth),
diff --git a/dom/canvas/OffscreenCanvas.h b/dom/canvas/OffscreenCanvas.h
index af201857ae26..c5dfb644190e 100644
--- a/dom/canvas/OffscreenCanvas.h
+++ b/dom/canvas/OffscreenCanvas.h
@@ -163,12 +163,10 @@ class OffscreenCanvas final : public DOMEventTargetHelper,
       nsCOMPtr<nsIGlobalObject>&& aGlobal, Promise* aPromise);
 
   void CanvasAttrChanged() {
-    mAttrDirty = true;
     ErrorResult dummy;
     UpdateContext(nullptr, JS::NullHandleValue, dummy);
   }
 
-  bool mAttrDirty;
   bool mNeutered;
   bool mIsWriteOnly;
 
diff --git a/dom/canvas/OffscreenCanvasDisplayHelper.cpp b/dom/canvas/OffscreenCanvasDisplayHelper.cpp
index c8f05e6a8c66..8d75cff2f7a5 100644
--- a/dom/canvas/OffscreenCanvasDisplayHelper.cpp
+++ b/dom/canvas/OffscreenCanvasDisplayHelper.cpp
@@ -45,11 +45,21 @@ RefPtr<layers::ImageContainer> OffscreenCanvasDisplayHelper::GetImageContainer()
   return mImageContainer;
 }
 
+layers::CompositableHandle OffscreenCanvasDisplayHelper::GetCompositableHandle()
+    const {
+  MutexAutoLock lock(mMutex);
+  return mData.mHandle;
+}
+
 void OffscreenCanvasDisplayHelper::UpdateContext(
     CanvasContextType aType, const Maybe<int32_t>& aChildId) {
   MutexAutoLock lock(mMutex);
-  mImageContainer =
-      MakeRefPtr<layers::ImageContainer>(layers::ImageContainer::ASYNCHRONOUS);
+
+  if (aType != CanvasContextType::WebGPU) {
+    mImageContainer = MakeRefPtr<layers::ImageContainer>(
+        layers::ImageContainer::ASYNCHRONOUS);
+  }
+
   mType = aType;
   mContextChildId = aChildId;
 
@@ -82,6 +92,16 @@ bool OffscreenCanvasDisplayHelper::CommitFrameToCompositor(
     MaybeQueueInvalidateElement();
   }
 
+  if (mData.mHandle) {
+    // No need to update the ImageContainer as the presentation itself is
+    // handled in the compositor process.
+    return true;
+  }
+
+  if (!mImageContainer) {
+    return false;
+  }
+
   if (mData.mIsOpaque) {
     flags |= layers::TextureFlags::IS_OPAQUE;
     format = gfx::SurfaceFormat::B8G8R8X8;
diff --git a/dom/canvas/OffscreenCanvasDisplayHelper.h b/dom/canvas/OffscreenCanvasDisplayHelper.h
index 970f8c4be5d2..c28f9676b911 100644
--- a/dom/canvas/OffscreenCanvasDisplayHelper.h
+++ b/dom/canvas/OffscreenCanvasDisplayHelper.h
@@ -28,6 +28,7 @@ struct OffscreenCanvasDisplayData final {
   bool mIsOpaque = true;
   bool mIsAlphaPremult = true;
   mozilla::gl::OriginPos mOriginPos = gl::OriginPos::TopLeft;
+  mozilla::layers::CompositableHandle mHandle;
 };
 
 class OffscreenCanvasDisplayHelper final {
@@ -41,6 +42,8 @@ class OffscreenCanvasDisplayHelper final {
 
   RefPtr<layers::ImageContainer> GetImageContainer() const;
 
+  layers::CompositableHandle GetCompositableHandle() const;
+
   void UpdateContext(CanvasContextType aType, const Maybe<int32_t>& aChildId);
 
   bool CommitFrameToCompositor(nsICanvasRenderingContextInternal* aContext,
diff --git a/dom/html/HTMLCanvasElement.cpp b/dom/html/HTMLCanvasElement.cpp
index 8cc3fd8cac74..a49828db1fb6 100644
--- a/dom/html/HTMLCanvasElement.cpp
+++ b/dom/html/HTMLCanvasElement.cpp
@@ -1478,4 +1478,11 @@ webgpu::CanvasContext* HTMLCanvasElement::GetWebGPUContext() {
   return static_cast<webgpu::CanvasContext*>(GetCurrentContext());
 }
 
+CompositableHandle HTMLCanvasElement::GetCompositableHandle() const {
+  if (mOffscreenDisplay) {
+    return mOffscreenDisplay->GetCompositableHandle();
+  }
+  return CompositableHandle();
+}
+
 }  // namespace mozilla::dom
diff --git a/dom/html/HTMLCanvasElement.h b/dom/html/HTMLCanvasElement.h
index 3cd29b289955..a8625bdab5bf 100644
--- a/dom/html/HTMLCanvasElement.h
+++ b/dom/html/HTMLCanvasElement.h
@@ -347,6 +347,8 @@ class HTMLCanvasElement final : public nsGenericHTMLElement,
 
   layers::ImageContainer* GetImageContainer() const { return mImageContainer; }
 
+  layers::CompositableHandle GetCompositableHandle() const;
+
  protected:
   bool mResetLayer;
   bool mMaybeModified;  // we fetched the context, so we may have written to the
diff --git a/dom/webgpu/CanvasContext.cpp b/dom/webgpu/CanvasContext.cpp
index 7d30d06bd10f..d4b4689faad9 100644
--- a/dom/webgpu/CanvasContext.cpp
+++ b/dom/webgpu/CanvasContext.cpp
@@ -73,7 +73,14 @@ void CanvasContext::Configure(const dom::GPUCanvasConfiguration& aDesc) {
   // Force a new frame to be built, which will execute the
   // `CanvasContextType::WebGPU` switch case in `CreateWebRenderCommands` and
   // populate the WR user data.
-  mCanvasElement->InvalidateCanvas();
+  if (mCanvasElement) {
+    mCanvasElement->InvalidateCanvas();
+  } else if (mOffscreenCanvas) {
+    dom::OffscreenCanvasDisplayData data;
+    data.mSize = {mWidth, mHeight};
+    data.mHandle = mHandle;
+    mOffscreenCanvas->UpdateDisplayData(data);
+  }
 }
 
 void CanvasContext::Unconfigure() {
diff --git a/layout/generic/nsHTMLCanvasFrame.cpp b/layout/generic/nsHTMLCanvasFrame.cpp
index 15d62246592d..ad4fa3952c6a 100644
--- a/layout/generic/nsHTMLCanvasFrame.cpp
+++ b/layout/generic/nsHTMLCanvasFrame.cpp
@@ -108,27 +108,35 @@ class nsDisplayCanvas final : public nsPaintedDisplayItem {
     element->HandlePrintCallback(mFrame->PresContext());
 
     if (element->IsOffscreen()) {
-      // If we are offscreen, then we display via an ImageContainer which is
-      // updated asynchronously, likely from a worker thread. There is nothing
-      // to paint until the owner attaches it.
+      // If we are offscreen, then we either display via an ImageContainer
+      // which is updated asynchronously, likely from a worker thread, or a
+      // CompositableHandle managed inside the compositor process. There is
+      // nothing to paint until the owner attaches it.
+
+      nsHTMLCanvasFrame* canvasFrame = static_cast<nsHTMLCanvasFrame*>(mFrame);
+      nsIntSize canvasSizeInPx = canvasFrame->GetCanvasSize();
+      IntrinsicSize intrinsicSize = IntrinsicSizeFromCanvasSize(canvasSizeInPx);
+      AspectRatio intrinsicRatio = IntrinsicRatioFromCanvasSize(canvasSizeInPx);
+      nsRect area = mFrame->GetContentRectRelativeToSelf() + ToReferenceFrame();
+      nsRect dest = nsLayoutUtils::ComputeObjectDestRect(
+          area, intrinsicSize, intrinsicRatio, mFrame->StylePosition());
+      LayoutDeviceRect bounds = LayoutDeviceRect::FromAppUnits(
+          dest, mFrame->PresContext()->AppUnitsPerDevPixel());
+
       RefPtr<ImageContainer> container = element->GetImageContainer();
       if (container) {
-        nsHTMLCanvasFrame* canvasFrame =
-            static_cast<nsHTMLCanvasFrame*>(mFrame);
-        nsIntSize canvasSizeInPx = canvasFrame->GetCanvasSize();
-        IntrinsicSize intrinsicSize =
-            IntrinsicSizeFromCanvasSize(canvasSizeInPx);
-        AspectRatio intrinsicRatio =
-            IntrinsicRatioFromCanvasSize(canvasSizeInPx);
-        nsRect area =
-            mFrame->GetContentRectRelativeToSelf() + ToReferenceFrame();
-        nsRect dest = nsLayoutUtils::ComputeObjectDestRect(
-            area, intrinsicSize, intrinsicRatio, mFrame->StylePosition());
-        LayoutDeviceRect bounds = LayoutDeviceRect::FromAppUnits(
-            dest, mFrame->PresContext()->AppUnitsPerDevPixel());
         aManager->CommandBuilder().PushImage(this, container, aBuilder,
                                              aResources, aSc, bounds, bounds);
+        return true;
       }
+
+      CompositableHandle handle = element->GetCompositableHandle();
+      if (handle) {
+        aManager->CommandBuilder().PushInProcessImage(this, handle, aBuilder,
+                                                      aResources, aSc, bounds);
+        return true;
+      }
+
       return true;
     }