diff --git a/src/System.Windows.Forms/PublicAPI.Unshipped.txt b/src/System.Windows.Forms/PublicAPI.Unshipped.txt
index 3348c917404..904ff4f1046 100644
--- a/src/System.Windows.Forms/PublicAPI.Unshipped.txt
+++ b/src/System.Windows.Forms/PublicAPI.Unshipped.txt
@@ -1,3 +1,4 @@
+override System.Windows.Forms.Button.BackgroundImage.set -> void
 static System.Windows.Forms.Application.SetColorMode(System.Windows.Forms.SystemColorMode systemColorMode) -> void
 static System.Windows.Forms.TaskDialog.ShowDialogAsync(nint hwndOwner, System.Windows.Forms.TaskDialogPage! page, System.Windows.Forms.TaskDialogStartupLocation startupLocation = System.Windows.Forms.TaskDialogStartupLocation.CenterOwner) -> System.Threading.Tasks.Task<System.Windows.Forms.TaskDialogButton!>!
 static System.Windows.Forms.TaskDialog.ShowDialogAsync(System.Windows.Forms.IWin32Window! owner, System.Windows.Forms.TaskDialogPage! page, System.Windows.Forms.TaskDialogStartupLocation startupLocation = System.Windows.Forms.TaskDialogStartupLocation.CenterOwner) -> System.Threading.Tasks.Task<System.Windows.Forms.TaskDialogButton!>!
diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/Button.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/Button.cs
index e76dd755f29..6eada6bc3d9 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/Button.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/Button.cs
@@ -148,6 +148,21 @@ public virtual DialogResult DialogResult
         }
     }
 
+    public override Image? BackgroundImage
+    {
+        set
+        {
+            base.BackgroundImage = value;
+
+            if (Application.IsDarkModeEnabled)
+            {
+                // BackgroundImage changes may affect rendering logic,
+                // so we manually update the OwnerDraw flag to ensure correct visual behavior.
+                UpdateOwnerDraw();
+            }
+        }
+    }
+
     /// <summary>
     ///  Defines, whether the control is owner-drawn. Based on this,
     ///  the UserPaint flags get set, which in turn makes it later
@@ -161,7 +176,6 @@ private protected override bool OwnerDraw
         get
         {
             if (Application.IsDarkModeEnabled
-
                 // The SystemRenderer cannot render images. So, we flip to our
                 // own DarkMode renderer, if we need to render images, except if...
                 && Image is null
diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/ButtonBaseAdapter.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/ButtonBaseAdapter.cs
index 39b5b0ab852..9e97f45b584 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/ButtonBaseAdapter.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/ButtonBaseAdapter.cs
@@ -547,21 +547,6 @@ internal void PaintField(
     /// </summary>
     internal void PaintImage(PaintEventArgs e, LayoutData layout)
     {
-        if (Application.IsDarkModeEnabled && Control.DarkModeRequestState is true && Control.BackgroundImage is not null)
-        {
-            Rectangle bounds = Control.ClientRectangle;
-            bounds.Inflate(-ButtonBorderSize, -ButtonBorderSize);
-            ControlPaint.DrawBackgroundImage(
-                e.GraphicsInternal,
-                Control.BackgroundImage,
-                Color.Transparent,
-                Control.BackgroundImageLayout,
-                Control.ClientRectangle,
-                bounds,
-                Control.DisplayRectangle.Location,
-                Control.RightToLeft);
-        }
-
         if (Control.Image is not null)
         {
             // Setup new clip region & draw
diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeAdapter.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeAdapter.cs
index a85dd3ed4cc..34458e21981 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeAdapter.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeAdapter.cs
@@ -70,6 +70,32 @@ private Color GetButtonBackColor(PushButtonState state)
         return backColor;
     }
 
+    internal void PaintBackgroundImage(PaintEventArgs e, int borderSize, Rectangle paddedBounds)
+    {
+        if (Control.BackgroundImage is not null)
+        {
+            Rectangle bounds = paddedBounds;
+            if (Control.FlatStyle == FlatStyle.Flat)
+            {
+                bounds.Inflate(-borderSize - 1, -borderSize - 1);
+            }
+            else
+            {
+                bounds.Inflate(-1, -1);
+            }
+
+            ControlPaint.DrawBackgroundImage(
+                e.GraphicsInternal,
+                Control.BackgroundImage,
+                Color.Transparent,
+                Control.BackgroundImageLayout,
+                paddedBounds,
+                bounds,
+                bounds.Location,
+                Control.RightToLeft);
+        }
+    }
+
     internal override void PaintUp(PaintEventArgs e, CheckState state)
     {
         try
@@ -93,6 +119,10 @@ internal override void PaintUp(PaintEventArgs e, CheckState state)
                 Control.Parent?.BackColor ?? Control.BackColor,
                 GetButtonBackColor(pushButtonState),
                 _ => PaintImage(e, layout),
+                _ => PaintBackgroundImage(
+                    e,
+                    Control.FlatAppearance.BorderSize,
+                    Control.ClientRectangle),
                 () => PaintField(
                     e,
                     layout,
@@ -131,6 +161,10 @@ internal override void PaintDown(PaintEventArgs e, CheckState state)
                 Control.Parent?.BackColor ?? Control.BackColor,
                 GetButtonBackColor(PushButtonState.Pressed),
                 _ => PaintImage(e, layout),
+                _ => PaintBackgroundImage(
+                    e,
+                    Control.FlatAppearance.BorderSize,
+                    Control.ClientRectangle),
                 () => PaintField(
                     e,
                     layout,
@@ -169,6 +203,10 @@ internal override void PaintOver(PaintEventArgs e, CheckState state)
                 Control.Parent?.BackColor ?? Control.BackColor,
                 GetButtonBackColor(PushButtonState.Hot),
                 _ => PaintImage(e, layout),
+                _ => PaintBackgroundImage(
+                    e,
+                    Control.FlatAppearance.BorderSize,
+                    Control.ClientRectangle),
                 () => PaintField(
                     e,
                     layout,
diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeRendererBase.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeRendererBase.cs
index 9d655a618b0..55897ec79d7 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeRendererBase.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/ButtonDarkModeRendererBase.cs
@@ -39,6 +39,7 @@ public void RenderButton(
         Color parentBackgroundColor,
         Color backColor,
         Action<Rectangle> paintImage,
+        Action<Rectangle> paintBackgroundImage,
         Action paintField)
     {
         ArgumentNullException.ThrowIfNull(graphics);
@@ -63,6 +64,8 @@ public void RenderButton(
             // Draw button background and get content bounds
             Rectangle contentBounds = DrawButtonBackground(graphics, paddedBounds, state, isDefault, backColor);
 
+            paintBackgroundImage(paddedBounds);
+
             // Paint image and field using the provided delegates
             paintImage(contentBounds);
 
diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/IButtonRenderer.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/IButtonRenderer.cs
index ab1f7844042..5490b7c069f 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/IButtonRenderer.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/Buttons/ButtonInternal/DarkMode/IButtonRenderer.cs
@@ -50,6 +50,7 @@ void RenderButton(
         Color parentBackgroundColor,
         Color backColor,
         Action<Rectangle> paintImage,
+        Action<Rectangle> paintBackgroundImage,
         Action paintField);
 
     /// <summary>