diff --git a/src/System.Windows.Forms/src/System/Windows/Forms/Control.cs b/src/System.Windows.Forms/src/System/Windows/Forms/Control.cs
index 64e8562c4fd..74768e63256 100644
--- a/src/System.Windows.Forms/src/System/Windows/Forms/Control.cs
+++ b/src/System.Windows.Forms/src/System/Windows/Forms/Control.cs
@@ -9629,6 +9629,9 @@ internal virtual void RecreateHandleCore()
                     // the call shouldn't fail.
                     // However, it could fail if this.CreateParams.Parent is changed outside our control.
                     CreateHandle();
+
+                    // DestroyHandle resets the state, but CreateHandle doesn't set the state back.
+                    SetState(States.Created, true);
                 }
                 catch (Exception)
                 {
diff --git a/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ControlTests.cs b/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ControlTests.cs
index 2c5b6d5a4a9..9f0f78df088 100644
--- a/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ControlTests.cs
+++ b/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ControlTests.cs
@@ -722,6 +722,62 @@ public void Control_CreateParams_GetVisible_ReturnsExpected(bool visible, int ex
             Assert.False(control.IsHandleCreated);
         }
 
+        [WinFormsFact]
+        public void Control_RecreateHandleCore_invokes_OnParentHandleRecreated_for_children()
+        {
+            using Form form = new();
+            SubCheckedListBox checkedListBox1 = new();
+            SubButton button1 = new();
+            SubListBox listBox1 = new();
+            SubListView listView1 = new();
+
+            checkedListBox1.Items.AddRange(new object[] { "Foo", "Foo", "Foo" });
+            checkedListBox1.Location = new Point(10, 10);
+            checkedListBox1.Size = new Size(103, 64);
+
+            button1.Location = new Point(12, 166);
+            button1.Size = new Size(213, 20);
+
+            listBox1.Items.AddRange(new object[] { "Foo", "Foo", "Foo" });
+            listBox1.Location = new Point(12, 80);
+            listBox1.Size = new Size(101, 69);
+
+            listView1.Items.AddRange(new ListViewItem[] { new("Foo"), new("Foo"), new("Foo") });
+            listView1.Location = new Point(130, 10);
+            listView1.Size = new Size(121, 64);
+            listView1.View = View.List;
+
+            form.Controls.Add(checkedListBox1);
+            form.Controls.Add(button1);
+            form.Controls.Add(listBox1);
+            form.Controls.Add(listView1);
+
+            form.Show();
+
+            // This will recreate the handle.
+            form.ShowInTaskbar = false;
+
+            try
+            {
+                AssertHandler(button1);
+                AssertHandler(listView1);
+                AssertHandler(checkedListBox1);
+                AssertHandler(listBox1);
+            }
+            finally
+            {
+                form.Close();
+            }
+
+            return;
+
+            static void AssertHandler(IParentHandleRecreationHandler handler)
+            {
+                Assert.Equal(1, handler.OnParentHandleRecreatedCalled);
+                Assert.Equal(1, handler.OnParentHandleRecreatingCalled);
+            }
+        }
+
         private class SubControl : Control
         {
             public SubControl() : base()
@@ -1046,5 +1102,83 @@ public SubControl(Control parent, string text, int left, int top, int width, int
 
             public new void WndProc(ref Message m) => base.WndProc(ref m);
         }
+
+        private class SubCheckedListBox : CheckedListBox, IParentHandleRecreationHandler
+        {
+            public int OnParentHandleRecreatedCalled { get; private set; }
+            public int OnParentHandleRecreatingCalled { get; private set; }
+
+            internal override void OnParentHandleRecreated()
+            {
+                OnParentHandleRecreatedCalled++;
+                base.OnParentHandleRecreated();
+            }
+
+            internal override void OnParentHandleRecreating()
+            {
+                OnParentHandleRecreatingCalled++;
+                base.OnParentHandleRecreating();
+            }
+        }
+
+        private class SubListBox : ListBox, IParentHandleRecreationHandler
+        {
+            public int OnParentHandleRecreatedCalled { get; private set; }
+            public int OnParentHandleRecreatingCalled { get; private set; }
+
+            internal override void OnParentHandleRecreated()
+            {
+                OnParentHandleRecreatedCalled++;
+                base.OnParentHandleRecreated();
+            }
+
+            internal override void OnParentHandleRecreating()
+            {
+                OnParentHandleRecreatingCalled++;
+                base.OnParentHandleRecreating();
+            }
+        }
+
+        private class SubButton : Button, IParentHandleRecreationHandler
+        {
+            public int OnParentHandleRecreatedCalled { get; private set; }
+            public int OnParentHandleRecreatingCalled { get; private set; }
+
+            internal override void OnParentHandleRecreated()
+            {
+                OnParentHandleRecreatedCalled++;
+                base.OnParentHandleRecreated();
+            }
+
+            internal override void OnParentHandleRecreating()
+            {
+                OnParentHandleRecreatingCalled++;
+                base.OnParentHandleRecreating();
+            }
+        }
+
+        private class SubListView : ListView, IParentHandleRecreationHandler
+        {
+            public int OnParentHandleRecreatedCalled { get; private set; }
+            public int OnParentHandleRecreatingCalled { get; private set; }
+
+            internal override void OnParentHandleRecreated()
+            {
+                OnParentHandleRecreatedCalled++;
+                base.OnParentHandleRecreated();
+            }
+
+            internal override void OnParentHandleRecreating()
+            {
+                OnParentHandleRecreatingCalled++;
+                base.OnParentHandleRecreating();
+            }
+        }
+
+        private interface IParentHandleRecreationHandler
+        {
+            int OnParentHandleRecreatedCalled { get; }
+            int OnParentHandleRecreatingCalled { get; }
+        }
     }
 }