diff --git a/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.NativeImageList.cs b/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.NativeImageList.cs
index 800304c3e41..5ae55105cf8 100644
--- a/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.NativeImageList.cs
+++ b/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.NativeImageList.cs
@@ -61,6 +61,9 @@ private void Init(IntPtr himl)
 
             public void Dispose()
             {
+#if DEBUG
+                GC.SuppressFinalize(this);
+#endif
                 lock (s_syncLock)
                 {
                     if (Handle == IntPtr.Zero)
@@ -68,13 +71,10 @@ public void Dispose()
                         return;
                     }
 
-                    ComCtl32.ImageList.Destroy(Handle);
+                    var result = ComCtl32.ImageList.Destroy(Handle);
+                    Debug.Assert(result.IsTrue());
                     Handle = IntPtr.Zero;
                 }
-
-#if DEBUG
-                GC.SuppressFinalize(this);
-#endif
             }
 
 #if DEBUG
@@ -91,6 +91,13 @@ public void Dispose()
             }
 #endif
 
+            internal IntPtr TransferOwnership()
+            {
+                var handle = Handle;
+                Handle = IntPtr.Zero;
+                return handle;
+            }
+
             internal NativeImageList Duplicate()
             {
                 lock (s_syncLock)
diff --git a/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.cs b/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.cs
index 5670a99d6a8..9e44835c61b 100644
--- a/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.cs
+++ b/src/System.Windows.Forms/src/System/Windows/Forms/ImageList.cs
@@ -142,6 +142,17 @@ public IntPtr Handle
             }
         }
 
+        internal IntPtr CreateUniqueHandle()
+        {
+            if (_nativeImageList == null)
+            {
+                CreateHandle();
+            }
+
+            using var iml = _nativeImageList.Duplicate();
+            return iml.TransferOwnership();
+        }
+
         /// <summary>
         ///  Whether or not the underlying Win32 handle has been created.
         /// </summary>
diff --git a/src/System.Windows.Forms/src/System/Windows/Forms/ListView.cs b/src/System.Windows.Forms/src/System/Windows/Forms/ListView.cs
index 2d8353f0741..a9add845ed2 100644
--- a/src/System.Windows.Forms/src/System/Windows/Forms/ListView.cs
+++ b/src/System.Windows.Forms/src/System/Windows/Forms/ListView.cs
@@ -579,11 +579,21 @@ public bool CheckBoxes
                         {
                             if (CheckBoxes)
                             { // we want custom checkboxes
-                                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, _imageListState.Handle);
+                                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, _imageListState.CreateUniqueHandle());
+                                if (previousHandle != IntPtr.Zero)
+                                {
+                                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                                    Debug.Assert(result.IsTrue());
+                                }
                             }
                             else
                             {
-                                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, IntPtr.Zero);
+                                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, IntPtr.Zero);
+                                if (previousHandle != IntPtr.Zero)
+                                {
+                                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                                    Debug.Assert(result.IsTrue());
+                                }
                             }
                         }
 
@@ -664,7 +674,9 @@ protected override CreateParams CreateParams
                     cp.Style |= (currentStyle & (int)(User32.WS.HSCROLL | User32.WS.VSCROLL));
                 }
 
-                cp.Style |= (int)LVS.SHAREIMAGELISTS;
+                // disabled until ownership management of list handles is fixed
+                // https://github.com/dotnet/winforms/issues/3531
+                //cp.Style |= (int)LVS.SHAREIMAGELISTS;
 
                 switch (alignStyle)
                 {
@@ -966,8 +978,13 @@ public ImageList GroupImageList
                     return;
                 }
 
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.GROUPHEADER,
-                        value is null ? IntPtr.Zero : value.Handle);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.GROUPHEADER,
+                        value is null ? IntPtr.Zero : value.CreateUniqueHandle());
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
             }
         }
 
@@ -1235,7 +1252,13 @@ public ImageList LargeImageList
                     return;
                 }
 
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.NORMAL, value is null ? IntPtr.Zero : value.Handle);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.NORMAL, value is null ? IntPtr.Zero : value.CreateUniqueHandle());
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
+
                 if (AutoArrange && !listViewState1[LISTVIEWSTATE1_disposingImageLists])
                 {
                     UpdateListViewItemsLocations();
@@ -1474,7 +1497,12 @@ public ImageList SmallImageList
                     return;
                 }
 
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.SMALL, value is null ? IntPtr.Zero : value.Handle);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.SMALL, value is null ? IntPtr.Zero : value.CreateUniqueHandle());
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
 
                 if (View == View.SmallIcon)
                 {
@@ -1582,7 +1610,12 @@ public ImageList StateImageList
 
                     if (IsHandleCreated)
                     {
-                        User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, value is null ? IntPtr.Zero : value.Handle);
+                        var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, value is null ? IntPtr.Zero : value.CreateUniqueHandle());
+                        if (previousHandle != IntPtr.Zero)
+                        {
+                            var result = ComCtl32.ImageList.Destroy(previousHandle);
+                            Debug.Assert(result.IsTrue());
+                        }
                     }
                 }
                 else
@@ -1597,7 +1630,12 @@ public ImageList StateImageList
                         // (Yes, it does exactly that even though our wrapper sets LVS_SHAREIMAGELISTS on the native listView.)
                         // So we make the native listView forget about its StateImageList just before we recreate the handle.
                         // Likely related to https://devblogs.microsoft.com/oldnewthing/20171128-00/?p=97475
-                        User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, IntPtr.Zero);
+                        var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, IntPtr.Zero);
+                        if (previousHandle != IntPtr.Zero)
+                        {
+                            var result = ComCtl32.ImageList.Destroy(previousHandle);
+                            Debug.Assert(result.IsTrue());
+                        }
                     }
 
                     _imageListState = value;
@@ -1615,8 +1653,13 @@ public ImageList StateImageList
                     }
                     else
                     {
-                        User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE,
-                            (_imageListState is null || _imageListState.Images.Count == 0) ? IntPtr.Zero : _imageListState.Handle);
+                        var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE,
+                            (_imageListState is null || _imageListState.Images.Count == 0) ? IntPtr.Zero : _imageListState.CreateUniqueHandle());
+                        if (previousHandle != IntPtr.Zero)
+                        {
+                            var result = ComCtl32.ImageList.Destroy(previousHandle);
+                            Debug.Assert(result.IsTrue());
+                        }
                     }
 
                     // Comctl should handle auto-arrange for us, but doesn't
@@ -3672,8 +3715,13 @@ private void GroupImageListRecreateHandle(object sender, EventArgs e)
                 return;
             }
 
-            IntPtr handle = (GroupImageList is null) ? IntPtr.Zero : GroupImageList.Handle;
-            User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.GROUPHEADER, handle);
+            IntPtr handle = (GroupImageList is null) ? IntPtr.Zero : GroupImageList.CreateUniqueHandle();
+            var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.GROUPHEADER, handle);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
         }
 
         public ListViewHitTestInfo HitTest(Point point)
@@ -4243,8 +4291,13 @@ private void LargeImageListRecreateHandle(object sender, EventArgs e)
                 return;
             }
 
-            IntPtr handle = (LargeImageList is null) ? IntPtr.Zero : LargeImageList.Handle;
-            User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.NORMAL, handle);
+            IntPtr handle = (LargeImageList is null) ? IntPtr.Zero : LargeImageList.CreateUniqueHandle();
+            var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.NORMAL, handle);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
 
             ForceCheckBoxUpdate();
         }
@@ -4587,6 +4640,34 @@ protected override void OnHandleCreated(EventArgs e)
 
         protected override void OnHandleDestroyed(EventArgs e)
         {
+            var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.NORMAL);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
+
+            previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.SMALL);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
+
+            previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
+
+            previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.GROUPHEADER);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
+
             // don't save the list view items state when in virtual mode : it is the responsability of the
             // user to cache the list view items in virtual mode
             if (!Disposing && !VirtualMode)
@@ -4822,22 +4903,42 @@ protected void RealizeProperties()
 
             if (_imageListLarge != null)
             {
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.NORMAL, _imageListLarge.Handle);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.NORMAL, _imageListLarge.CreateUniqueHandle());
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
             }
 
             if (_imageListSmall != null)
             {
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.SMALL, _imageListSmall.Handle);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.SMALL, _imageListSmall.CreateUniqueHandle());
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
             }
 
             if (_imageListState != null)
             {
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, _imageListState.Handle);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, _imageListState.CreateUniqueHandle());
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
             }
 
             if (_imageListGroup != null)
             {
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.GROUPHEADER, _imageListGroup.Handle);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.GROUPHEADER, _imageListGroup.CreateUniqueHandle());
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
             }
         }
 
@@ -5364,8 +5465,13 @@ private void SmallImageListRecreateHandle(object sender, EventArgs e)
                 return;
             }
 
-            IntPtr handle = (SmallImageList is null) ? IntPtr.Zero : SmallImageList.Handle;
-            User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.SMALL, handle);
+            IntPtr handle = (SmallImageList is null) ? IntPtr.Zero : SmallImageList.CreateUniqueHandle();
+            var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.SMALL, handle);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
 
             ForceCheckBoxUpdate();
         }
@@ -5396,8 +5502,13 @@ private void StateImageListRecreateHandle(object sender, EventArgs e)
                 return;
             }
 
-            IntPtr handle = (StateImageList is null) ? IntPtr.Zero : StateImageList.Handle;
-            User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, handle);
+            IntPtr handle = (StateImageList is null) ? IntPtr.Zero : StateImageList.CreateUniqueHandle();
+            var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, handle);
+            if (previousHandle != IntPtr.Zero)
+            {
+                var result = ComCtl32.ImageList.Destroy(previousHandle);
+                Debug.Assert(result.IsTrue());
+            }
         }
 
         /// <summary>
@@ -6164,7 +6275,12 @@ internal void RecreateHandleInternal()
             // (Yes, it does exactly that even though our wrapper sets LVS_SHAREIMAGELISTS on the native listView.)
             if (IsHandleCreated && StateImageList != null)
             {
-                User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, IntPtr.Zero);
+                var previousHandle = User32.SendMessageW(this, (User32.WM)LVM.SETIMAGELIST, (IntPtr)LVSIL.STATE, IntPtr.Zero);
+                if (previousHandle != IntPtr.Zero)
+                {
+                    var result = ComCtl32.ImageList.Destroy(previousHandle);
+                    Debug.Assert(result.IsTrue());
+                }
             }
 
             RecreateHandle();
diff --git a/src/System.Windows.Forms/src/System/Windows/Forms/TreeView.cs b/src/System.Windows.Forms/src/System/Windows/Forms/TreeView.cs
index ae8b7aad024..3c2b177ac3a 100644
--- a/src/System.Windows.Forms/src/System/Windows/Forms/TreeView.cs
+++ b/src/System.Windows.Forms/src/System/Windows/Forms/TreeView.cs
@@ -662,7 +662,7 @@ public ImageList ImageList
                                     value == null ? IntPtr.Zero : value.Handle);
                         if (StateImageList != null && StateImageList.Images.Count > 0 && internalStateImageList != null)
                         {
-                            SetStateImageList(internalStateImageList.Handle);
+                            SetStateImageList(internalStateImageList.CreateUniqueHandle());
                         }
                     }
                     UpdateCheckedState(root, true);
@@ -1819,7 +1819,7 @@ private void StateImageListRecreateHandle(object sender, EventArgs e)
                 IntPtr handle = IntPtr.Zero;
                 if (internalStateImageList != null)
                 {
-                    handle = internalStateImageList.Handle;
+                    handle = internalStateImageList.CreateUniqueHandle();
                 }
                 SetStateImageList(handle);
             }
@@ -1859,7 +1859,7 @@ private void StateImageListChangedHandle(object sender, EventArgs e)
                             internalStateImageList.ImageSize = (Size)ScaledStateImageSize;
                         }
 
-                        SetStateImageList(internalStateImageList.Handle);
+                        SetStateImageList(internalStateImageList.CreateUniqueHandle());
                     }
                 }
                 else //stateImageList == null || stateImageList.Images.Count = 0;
@@ -2050,7 +2050,7 @@ private void UpdateNativeStateImageList()
                     images[i] = stateImageList.Images[i - 1];
                 }
                 newImageList.Images.AddRange(images);
-                User32.SendMessageW(this, (User32.WM)TVM.SETIMAGELIST, (IntPtr)TVSIL.STATE, newImageList.Handle);
+                User32.SendMessageW(this, (User32.WM)TVM.SETIMAGELIST, (IntPtr)TVSIL.STATE, newImageList.CreateUniqueHandle());
 
                 if (internalStateImageList != null)
                 {
@@ -2067,7 +2067,8 @@ private void SetStateImageList(IntPtr handle)
             IntPtr handleOld = User32.SendMessageW(this, (User32.WM)TVM.SETIMAGELIST, (IntPtr)TVSIL.STATE, handle);
             if ((handleOld != IntPtr.Zero) && (handleOld != handle))
             {
-                ComCtl32.ImageList.Destroy(new HandleRef(this, handleOld));
+                var result = ComCtl32.ImageList.Destroy(new HandleRef(this, handleOld));
+                Debug.Assert(result.IsTrue());
             }
         }
 
@@ -2078,7 +2079,8 @@ private void DestroyNativeStateImageList(bool reset)
             IntPtr handle = User32.SendMessageW(this, (User32.WM)TVM.GETIMAGELIST, (IntPtr)TVSIL.STATE);
             if (handle != IntPtr.Zero)
             {
-                ComCtl32.ImageList.Destroy(new HandleRef(this, handle));
+                var result = ComCtl32.ImageList.Destroy(new HandleRef(this, handle));
+                Debug.Assert(result.IsTrue());
                 if (reset)
                 {
                     User32.SendMessageW(this, (User32.WM)TVM.SETIMAGELIST, (IntPtr)TVSIL.STATE);
@@ -2619,7 +2621,7 @@ internal override void UpdateStylesCore()
                     // user's images.
                     if (internalStateImageList != null)
                     {
-                        SetStateImageList(internalStateImageList.Handle);
+                        SetStateImageList(internalStateImageList.CreateUniqueHandle());
                     }
                 }
             }
diff --git a/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ListViewTests.cs b/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ListViewTests.cs
index 3d655d373e9..c3330b37db4 100644
--- a/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ListViewTests.cs
+++ b/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ListViewTests.cs
@@ -170,7 +170,9 @@ public void ListView_CreateParams_GetDefault_ReturnsExpected()
             Assert.Equal(97, createParams.Height);
             Assert.Equal(IntPtr.Zero, createParams.Parent);
             Assert.Null(createParams.Param);
-            Assert.Equal(0x56010148, createParams.Style);
+            // LVS.SHAREIMAGELISTS is temporarily removed from style until ownership management is fixed
+            // https://github.com/dotnet/winforms/issues/3531
+            Assert.Equal(0x56010108, createParams.Style);
             Assert.Equal(121, createParams.Width);
             Assert.Equal(0, createParams.X);
             Assert.Equal(0, createParams.Y);