diff --git chrome/browser/ui/views/chrome_javascript_app_modal_view_factory_views.cc chrome/browser/ui/views/chrome_javascript_app_modal_view_factory_views.cc
index b169371e4d42f..509e4bda85b47 100644
--- chrome/browser/ui/views/chrome_javascript_app_modal_view_factory_views.cc
+++ chrome/browser/ui/views/chrome_javascript_app_modal_view_factory_views.cc
@@ -100,7 +100,7 @@ javascript_dialogs::AppModalDialogView* CreateViewsJavaScriptDialog(
   gfx::NativeWindow parent_window =
       controller->web_contents()->GetTopLevelNativeWindow();
 #if defined(USE_AURA)
-  if (!parent_window->GetRootWindow()) {
+  if (parent_window && !parent_window->GetRootWindow()) {
     // When we are part of a WebContents that isn't actually being displayed
     // on the screen, we can't actually attach to it.
     parent_window = nullptr;
diff --git components/constrained_window/constrained_window_views.cc components/constrained_window/constrained_window_views.cc
index dc648ad1ae595..70698ed848990 100644
--- components/constrained_window/constrained_window_views.cc
+++ components/constrained_window/constrained_window_views.cc
@@ -101,15 +101,24 @@ void UpdateModalDialogPosition(views::Widget* widget,
   if (widget->HasCapture())
     return;
 
+  // |host_view| will be nullptr with CEF windowless rendering.
+  auto host_view = dialog_host->GetHostView();
   views::Widget* host_widget =
-      views::Widget::GetWidgetForNativeView(dialog_host->GetHostView());
+      host_view ? views::Widget::GetWidgetForNativeView(host_view) : nullptr;
 
   // If the host view is not backed by a Views::Widget, just update the widget
   // size. This can happen on MacViews under the Cocoa browser where the window
   // modal dialogs are displayed as sheets, and their position is managed by a
   // ConstrainedWindowSheetController instance.
   if (!host_widget) {
+#if BUILDFLAG(IS_MAC)
     widget->SetSize(size);
+#elif BUILDFLAG(IS_POSIX)
+    // Set the bounds here instead of relying on the default behavior of
+    // DesktopWindowTreeHostPlatform::CenterWindow which incorrectly centers
+    // the window on the screen.
+    widget->SetBounds(gfx::Rect(dialog_host->GetDialogPosition(size), size));
+#endif
     return;
   }
 
@@ -215,7 +224,8 @@ views::Widget* CreateWebModalDialogViews(views::WidgetDelegate* dialog,
 
   return views::DialogDelegate::CreateDialogWidget(
       dialog, nullptr,
-      manager->delegate()->GetWebContentsModalDialogHost()->GetHostView());
+      manager->delegate()->GetWebContentsModalDialogHost()->GetHostView(),
+      manager->delegate()->GetWebContentsModalDialogHost()->GetHostWidget());
 }
 
 views::Widget* CreateBrowserModalDialogViews(
@@ -232,8 +242,13 @@ views::Widget* CreateBrowserModalDialogViews(views::DialogDelegate* dialog,
 
   gfx::NativeView parent_view =
       parent ? CurrentClient()->GetDialogHostView(parent) : nullptr;
+  // Use with CEF windowless rendering.
+  gfx::AcceleratedWidget parent_widget =
+      parent ? gfx::kNullAcceleratedWidget :
+               CurrentClient()->GetModalDialogHost(parent)->GetHostWidget();
   views::Widget* widget =
-      views::DialogDelegate::CreateDialogWidget(dialog, nullptr, parent_view);
+      views::DialogDelegate::CreateDialogWidget(dialog, nullptr, parent_view,
+                                                parent_widget);
 
   bool requires_positioning = dialog->use_custom_frame();
 
@@ -246,8 +261,7 @@ views::Widget* CreateBrowserModalDialogViews(views::DialogDelegate* dialog,
   if (!requires_positioning)
     return widget;
 
-  ModalDialogHost* host =
-      parent ? CurrentClient()->GetModalDialogHost(parent) : nullptr;
+  ModalDialogHost* host = CurrentClient()->GetModalDialogHost(parent);
   if (host) {
     DCHECK_EQ(parent_view, host->GetHostView());
     ModalDialogHostObserver* dialog_host_observer =
diff --git components/constrained_window/native_web_contents_modal_dialog_manager_views.cc components/constrained_window/native_web_contents_modal_dialog_manager_views.cc
index 647391095306e..bd49316ac758e 100644
--- components/constrained_window/native_web_contents_modal_dialog_manager_views.cc
+++ components/constrained_window/native_web_contents_modal_dialog_manager_views.cc
@@ -184,9 +184,20 @@ void NativeWebContentsModalDialogManagerViews::HostChanged(
   if (host_) {
     host_->AddObserver(this);
 
-    for (auto* widget : observed_widgets_) {
-      views::Widget::ReparentNativeView(widget->GetNativeView(),
-                                        host_->GetHostView());
+    // |host_view| will be nullptr with CEF windowless rendering.
+    if (auto host_view = host_->GetHostView()) {
+      for (auto* widget : observed_widgets_) {
+#if defined(USE_AURA)
+        auto widget_view = widget->GetNativeView();
+        // Don't reparent between different root windows. Doing so causes
+        // issues with layout of dialogs containing Chrome browsers.
+        if (host_view->GetRootWindow() == widget_view->GetRootWindow()) {
+          views::Widget::ReparentNativeView(widget_view, host_view);
+        }
+#else
+        views::Widget::ReparentNativeView(widget->GetNativeView(), host_view);
+#endif
+      }
     }
 
     OnPositionRequiresUpdate();
diff --git components/web_modal/modal_dialog_host.h components/web_modal/modal_dialog_host.h
index 51ed6bcf6b540..9ae4737e0737e 100644
--- components/web_modal/modal_dialog_host.h
+++ components/web_modal/modal_dialog_host.h
@@ -34,6 +34,10 @@ class WEB_MODAL_EXPORT ModalDialogHost {
 
   // Returns the view against which the dialog is positioned and parented.
   virtual gfx::NativeView GetHostView() const = 0;
+  // Returns the widget against which the dialog is positioned and parented.
+  // Used with CEF windowless rendering.
+  virtual gfx::AcceleratedWidget GetHostWidget() const {
+      return gfx::kNullAcceleratedWidget; }
   // Gets the position for the dialog in coordinates relative to the host view.
   virtual gfx::Point GetDialogPosition(const gfx::Size& size) = 0;
   // Returns whether a dialog currently about to be shown should be activated.
diff --git ui/views/window/dialog_delegate.cc ui/views/window/dialog_delegate.cc
index cd6fa368d3960..3a1f64fd295c7 100644
--- ui/views/window/dialog_delegate.cc
+++ ui/views/window/dialog_delegate.cc
@@ -64,10 +64,12 @@ DialogDelegate::DialogDelegate() {
 // static
 Widget* DialogDelegate::CreateDialogWidget(WidgetDelegate* delegate,
                                            gfx::NativeWindow context,
-                                           gfx::NativeView parent) {
+                                           gfx::NativeView parent,
+                                           gfx::AcceleratedWidget parent_widget) {
   views::Widget* widget = new views::Widget;
   views::Widget::InitParams params =
-      GetDialogWidgetInitParams(delegate, context, parent, gfx::Rect());
+      GetDialogWidgetInitParams(delegate, context, parent, gfx::Rect(),
+                                parent_widget);
   widget->Init(std::move(params));
   return widget;
 }
@@ -76,17 +78,19 @@ Widget* DialogDelegate::CreateDialogWidget(WidgetDelegate* delegate,
 Widget* DialogDelegate::CreateDialogWidget(
     std::unique_ptr<WidgetDelegate> delegate,
     gfx::NativeWindow context,
-    gfx::NativeView parent) {
+    gfx::NativeView parent,
+    gfx::AcceleratedWidget parent_widget) {
   DCHECK(delegate->owned_by_widget());
-  return CreateDialogWidget(delegate.release(), context, parent);
+  return CreateDialogWidget(delegate.release(), context, parent, parent_widget);
 }
 
 // static
-bool DialogDelegate::CanSupportCustomFrame(gfx::NativeView parent) {
+bool DialogDelegate::CanSupportCustomFrame(gfx::NativeView parent,
+                                           gfx::AcceleratedWidget parent_widget) {
 #if (BUILDFLAG(IS_LINUX) || BUILDFLAG(IS_CHROMEOS)) && \
     BUILDFLAG(ENABLE_DESKTOP_AURA)
   // The new style doesn't support unparented dialogs on Linux desktop.
-  return parent != nullptr;
+  return parent != nullptr || parent_widget != gfx::kNullAcceleratedWidget;
 #else
   return true;
 #endif
@@ -97,14 +101,15 @@ Widget::InitParams DialogDelegate::GetDialogWidgetInitParams(
     WidgetDelegate* delegate,
     gfx::NativeWindow context,
     gfx::NativeView parent,
-    const gfx::Rect& bounds) {
+    const gfx::Rect& bounds,
+    gfx::AcceleratedWidget parent_widget) {
   views::Widget::InitParams params;
   params.delegate = delegate;
   params.bounds = bounds;
   DialogDelegate* dialog = delegate->AsDialogDelegate();
 
   if (dialog)
-    dialog->params_.custom_frame &= CanSupportCustomFrame(parent);
+    dialog->params_.custom_frame &= CanSupportCustomFrame(parent, parent_widget);
 
   if (!dialog || dialog->use_custom_frame()) {
     params.opacity = Widget::InitParams::WindowOpacity::kTranslucent;
@@ -117,6 +122,7 @@ Widget::InitParams DialogDelegate::GetDialogWidgetInitParams(
   }
   params.context = context;
   params.parent = parent;
+  params.parent_widget = parent_widget;
 #if !BUILDFLAG(IS_APPLE)
   // Web-modal (ui::MODAL_TYPE_CHILD) dialogs with parents are marked as child
   // widgets to prevent top-level window behavior (independent movement, etc).
diff --git ui/views/window/dialog_delegate.h ui/views/window/dialog_delegate.h
index 4d64cf4f40af7..1d77b1c152253 100644
--- ui/views/window/dialog_delegate.h
+++ ui/views/window/dialog_delegate.h
@@ -97,13 +97,18 @@ class VIEWS_EXPORT DialogDelegate : public WidgetDelegate {
   // your use case.
   static Widget* CreateDialogWidget(std::unique_ptr<WidgetDelegate> delegate,
                                     gfx::NativeWindow context,
-                                    gfx::NativeView parent);
+                                    gfx::NativeView parent,
+                                    gfx::AcceleratedWidget parent_widget =
+                                        gfx::kNullAcceleratedWidget);
   static Widget* CreateDialogWidget(WidgetDelegate* delegate,
                                     gfx::NativeWindow context,
-                                    gfx::NativeView parent);
+                                    gfx::NativeView parent,
+                                    gfx::AcceleratedWidget parent_widget =
+                                        gfx::kNullAcceleratedWidget);
 
   // Whether using custom dialog frame is supported for this dialog.
-  static bool CanSupportCustomFrame(gfx::NativeView parent);
+  static bool CanSupportCustomFrame(gfx::NativeView parent,
+                                    gfx::AcceleratedWidget parent_widget);
 
   // Returns the dialog widget InitParams for a given |context| or |parent|.
   // If |bounds| is not empty, used to initially place the dialog, otherwise
@@ -111,7 +116,9 @@ class VIEWS_EXPORT DialogDelegate : public WidgetDelegate {
   static Widget::InitParams GetDialogWidgetInitParams(WidgetDelegate* delegate,
                                                       gfx::NativeWindow context,
                                                       gfx::NativeView parent,
-                                                      const gfx::Rect& bounds);
+                                                      const gfx::Rect& bounds,
+                                                      gfx::AcceleratedWidget parent_widget =
+                                                          gfx::kNullAcceleratedWidget);
 
   // Returns a mask specifying which of the available DialogButtons are visible
   // for the dialog.