diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/ListView/ListView.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/ListView/ListView.cs
index f290e8ce8eb..78b96e859fa 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/ListView/ListView.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/ListView/ListView.cs
@@ -113,6 +113,7 @@ public partial class ListView : Control
     private ImageList? _imageListSmall;
     private ImageList? _imageListState;
     private ImageList? _imageListGroup;
+    private ImageList? _darkModeStateImageList;
 
     private MouseButtons _downButton;
     private int _itemCount;
@@ -3066,6 +3067,9 @@ protected override void Dispose(bool disposing)
             DetachGroupImageListHandlers();
             _imageListGroup = null;
 
+            _darkModeStateImageList?.Dispose();
+            _darkModeStateImageList = null;
+
             // Remove any ColumnHeaders contained in this control
             if (_columnHeaders is not null)
             {
@@ -4703,9 +4707,84 @@ private void ApplyDarkModeOnDemand()
                 columnHeaderHandle,
                 $"{DarkModeIdentifier}_{ItemsViewThemeIdentifier}",
                 null);
+
+            if (CheckBoxes)
+            {
+                UpdateDarkModeCheckBoxImages();
+            }
+        }
+    }
+
+    private void UpdateDarkModeCheckBoxImages()
+    {
+        if (_imageListState is not null || !CheckBoxes || !IsHandleCreated)
+        {
+            return;
+        }
+
+        _darkModeStateImageList?.Dispose();
+
+        int size = ScaleHelper.ScaleToInitialSystemDpi(16);
+
+        ImageList imageList = new()
+        {
+            ImageSize = new Size(size, size),
+            ColorDepth = ColorDepth.Depth32Bit,
+            TransparentColor = Color.Transparent
+        };
+
+        imageList.Images.Add(CreateDarkModeCheckBoxBitmap(isChecked: false, size));
+        imageList.Images.Add(CreateDarkModeCheckBoxBitmap(isChecked: true, size));
+
+        // Ensure the checkbox extended style is active before assigning our custom state imagelist,
+        // otherwise the style refresh may overwrite the list with the default light-themed images.
+        ForceCheckBoxUpdate();
+
+        PInvokeCore.SendMessage(
+            this,
+            PInvoke.LVM_SETIMAGELIST,
+            (WPARAM)PInvoke.LVSIL_STATE,
+            (LPARAM)imageList.Handle);
+
+        _darkModeStateImageList = imageList;
+
+        if (VirtualMode)
+        {
+            return;
+        }
+
+        if (Items.Count > 0)
+        {
+            const LIST_VIEW_ITEM_STATE_FLAGS stateMask = LIST_VIEW_ITEM_STATE_FLAGS.LVIS_STATEIMAGEMASK;
+
+            for (int i = 0; i < Items.Count; i++)
+            {
+                bool isChecked = Items[i].Checked;
+                int stateIndex = isChecked ? 2 : 1;
+
+                SetItemState(i, (LIST_VIEW_ITEM_STATE_FLAGS)(stateIndex << 12), stateMask);
+            }
+
+            PInvokeCore.SendMessage(
+                this,
+                PInvoke.LVM_REDRAWITEMS,
+                (WPARAM)0,
+                (LPARAM)(Items.Count - 1));
         }
     }
 
+    private Bitmap CreateDarkModeCheckBoxBitmap(bool isChecked, int size)
+    {
+        Bitmap bitmap = new(size, size);
+
+        using Graphics graphics = Graphics.FromImage(bitmap);
+        graphics.Clear(Color.Transparent);
+        CheckBoxState state = isChecked ? CheckBoxState.CheckedNormal : CheckBoxState.UncheckedNormal;
+        CheckBoxRenderer.DrawCheckBoxWithVisualStyles(graphics, new Point(0, 0), state, HWNDInternal);
+
+        return bitmap;
+    }
+
     protected override void OnHandleDestroyed(EventArgs e)
     {
         // don't save the list view items state when in virtual mode : it is the responsibility of the
diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/TreeView/TreeView.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/TreeView/TreeView.cs
index 4d6a3c53602..6958d9ec35f 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/TreeView/TreeView.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/TreeView/TreeView.cs
@@ -284,6 +284,7 @@ public bool CheckBoxes
                     if (CheckBoxes)
                     {
                         UpdateStyles();
+                        UpdateCheckBoxImages();
                     }
                     else
                     {
@@ -1869,6 +1870,7 @@ protected override void OnHandleCreated(EventArgs e)
             int style = (int)PInvokeCore.GetWindowLong(this, WINDOW_LONG_PTR_INDEX.GWL_STYLE);
             style |= (int)PInvoke.TVS_CHECKBOXES;
             PInvokeCore.SetWindowLong(this, WINDOW_LONG_PTR_INDEX.GWL_STYLE, style);
+            UpdateCheckBoxImages();
         }
 
         if (ShowNodeToolTips && !DesignMode)
@@ -1991,6 +1993,43 @@ private void UpdateNativeStateImageList()
         _internalStateImageList = newImageList;
     }
 
+    private void UpdateCheckBoxImages()
+    {
+        if (DesignMode || !IsHandleCreated || !CheckBoxes || _stateImageList is not null)
+        {
+            return;
+        }
+
+        int size = StateImageSize?.Width ?? ScaleHelper.ScaleToInitialSystemDpi(16);
+        ImageList imageList = new()
+        {
+            ImageSize = new Size(size, size),
+            ColorDepth = ColorDepth.Depth32Bit
+        };
+
+        using Bitmap uncheckedBitmap = new(size, size);
+        using (Graphics g = Graphics.FromImage(uncheckedBitmap))
+        {
+            CheckBoxRenderer.DrawCheckBoxWithVisualStyles(g, new Point(0, 0), CheckBoxState.UncheckedNormal, HWNDInternal);
+        }
+
+        using Bitmap checkedBitmap = new(size, size);
+        using (Graphics g = Graphics.FromImage(checkedBitmap))
+        {
+            CheckBoxRenderer.DrawCheckBoxWithVisualStyles(g, new Point(0, 0), CheckBoxState.CheckedNormal, HWNDInternal);
+        }
+
+        // TreeView uses 1-based indexing: index 0=placeholder, 1=unchecked, 2=checked
+        imageList.Images.Add(new Bitmap(size, size)); // Placeholder
+        imageList.Images.Add(uncheckedBitmap);
+        imageList.Images.Add(checkedBitmap);
+
+        SetStateImageList(imageList.Handle);
+
+        _internalStateImageList?.Dispose();
+        _internalStateImageList = imageList;
+    }
+
     private void SetStateImageList(IntPtr handle)
     {
         // In certain cases (TREEVIEWSTATE_checkBoxes) e.g., the Native TreeView leaks the imageList
@@ -3385,6 +3424,7 @@ protected override unsafe void WndProc(ref Message m)
             case PInvokeCore.WM_SYSCOLORCHANGE:
                 PInvokeCore.SendMessage(this, PInvoke.TVM_SETINDENT, (WPARAM)Indent);
                 base.WndProc(ref m);
+                UpdateCheckBoxImages();
                 break;
             case PInvokeCore.WM_SETFOCUS:
                 // If we get focus through the LButtonDown .. we might have done the validation...