diff --git a/src/System.Windows.Forms/System/Windows/Forms/Form.cs b/src/System.Windows.Forms/System/Windows/Forms/Form.cs
index c3900d09c6b..21e2a6a6360 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Form.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Form.cs
@@ -4965,6 +4965,14 @@ private void SetFormTitleProperties()
     {
         if (TopLevel && IsHandleCreated)
         {
+            // Re-apply the dark-mode title bar flag. DWM window attributes are not preserved
+            // across handle recreation, so DWMWA_USE_IMMERSIVE_DARK_MODE must be restored
+            // here alongside the other DWM attributes.
+            if (Application.ColorModeSet && DarkModeRequestState is true)
+            {
+                SetFormImmersiveDarkModeInternal(Application.IsDarkModeEnabled);
+            }
+
             if (Properties.TryGetValue(s_propFormBorderColor, out Color? formBorderColor))
             {
                 SetFormAttributeColorInternal(DWMWINDOWATTRIBUTE.DWMWA_BORDER_COLOR, formBorderColor.Value);
@@ -4987,6 +4995,16 @@ private void SetFormTitleProperties()
         }
     }
 
+    private unsafe void SetFormImmersiveDarkModeInternal(bool isDarkMode)
+    {
+        BOOL isDark = isDarkMode;
+        PInvoke.DwmSetWindowAttribute(
+            HWND,
+            DWMWINDOWATTRIBUTE.DWMWA_USE_IMMERSIVE_DARK_MODE,
+            &isDark,
+            (uint)sizeof(BOOL));
+    }
+
     /// <summary>
     ///  Removes a form from the list of owned forms. Also sets the owner of the
     ///  removed form to null.
diff --git a/src/test/unit/System.Windows.Forms/System/Windows/Forms/FormTests.cs b/src/test/unit/System.Windows.Forms/System/Windows/Forms/FormTests.cs
index 26574491052..624108d3bc7 100644
--- a/src/test/unit/System.Windows.Forms/System/Windows/Forms/FormTests.cs
+++ b/src/test/unit/System.Windows.Forms/System/Windows/Forms/FormTests.cs
@@ -6,6 +6,7 @@
 using System.ComponentModel;
 using System.Drawing;
 using Moq;
+using Windows.Win32.Graphics.Dwm;
 
 namespace System.Windows.Forms.Tests;
 
@@ -1886,6 +1887,124 @@ public void Form_ShowInTaskbar_SetFalse_GetReturnsExpected()
         Assert.Equal(expectedDialogResult, form.DialogResult);
     }
 
+    [WinFormsFact]
+    public void Form_RecreateHandle_ReappliesImmersiveDarkModeTitleBar()
+    {
+        // Regression for https://github.com/dotnet/winforms/issues/12582
+        // Avoid Application.SetColorMode — can hang in NotifySystemEventsOfColorChange
+        // after a form has created the SystemEvents broadcast window.
+
+        if (SystemInformation.HighContrast)
+        {
+            return;
+        }
+
+        var applicationAccessor = typeof(Application).TestAccessor.Dynamic;
+        SystemColorMode? previousColorMode = applicationAccessor.s_colorMode;
+
+        try
+        {
+            applicationAccessor.s_colorMode = SystemColorMode.Dark;
+            Assert.True(Application.ColorModeSet);
+            Assert.True(Application.IsDarkModeEnabled);
+
+            using Form form = new();
+            form.TestAccessor.Dynamic.DarkModeRequestState = true;
+
+            form.Show();
+            Assert.True(form.IsHandleCreated);
+
+            Assert.True(
+                TryGetUseImmersiveDarkMode(form.HWND, out bool darkBefore) && darkBefore,
+                "Expected immersive dark mode when the form is first shown.");
+
+            IntPtr handleBefore = form.Handle;
+
+            form.RightToLeft = RightToLeft.Yes;
+
+            Assert.True(form.IsHandleCreated);
+            Assert.NotEqual(handleBefore, form.Handle);
+
+            Assert.True(
+                TryGetUseImmersiveDarkMode(form.HWND, out bool darkAfter) && darkAfter,
+                "Expected immersive dark mode restored after handle recreation.");
+
+            form.Close();
+        }
+        finally
+        {
+            applicationAccessor.s_colorMode = previousColorMode;
+        }
+    }
+
+    [WinFormsFact]
+    public void Form_ShowInTaskbar_Change_ReappliesImmersiveDarkModeTitleBar()
+    {
+        // Regression for https://github.com/dotnet/winforms/issues/12992
+        // Same root cause as #12582: handle recreation must re-apply
+        // DWMWA_USE_IMMERSIVE_DARK_MODE via Form.SetFormTitleProperties.
+        // Avoid Application.SetColorMode — can hang in NotifySystemEventsOfColorChange.
+
+        if (SystemInformation.HighContrast)
+        {
+            return;
+        }
+
+        var applicationAccessor = typeof(Application).TestAccessor.Dynamic;
+        SystemColorMode? previousColorMode = applicationAccessor.s_colorMode;
+
+        try
+        {
+            applicationAccessor.s_colorMode = SystemColorMode.Dark;
+            Assert.True(Application.ColorModeSet);
+            Assert.True(Application.IsDarkModeEnabled);
+
+            using Form form = new()
+            {
+                ShowInTaskbar = true,
+            };
+            form.TestAccessor.Dynamic.DarkModeRequestState = true;
+
+            form.Show();
+            Assert.True(form.IsHandleCreated);
+
+            Assert.True(
+                TryGetUseImmersiveDarkMode(form.HWND, out bool darkBefore) && darkBefore,
+                "Expected immersive dark mode when the form is first shown.");
+
+            IntPtr handleBefore = form.Handle;
+
+            // Repro path from #12992 (toggle force recreate, same as product UI).
+            form.ShowInTaskbar = false;
+
+            Assert.True(form.IsHandleCreated);
+            Assert.NotEqual(handleBefore, form.Handle);
+
+            Assert.True(
+                TryGetUseImmersiveDarkMode(form.HWND, out bool darkAfter) && darkAfter,
+                "Expected immersive dark mode restored after ShowInTaskbar forces handle recreation.");
+
+            form.Close();
+        }
+        finally
+        {
+            applicationAccessor.s_colorMode = previousColorMode;
+        }
+    }
+
+    private static unsafe bool TryGetUseImmersiveDarkMode(HWND hwnd, out bool isDark)
+    {
+        BOOL value = false;
+        HRESULT hr = PInvoke.DwmGetWindowAttribute(
+            hwnd,
+            DWMWINDOWATTRIBUTE.DWMWA_USE_IMMERSIVE_DARK_MODE,
+            &value,
+            (uint)sizeof(BOOL));
+
+        isDark = value;
+        return hr.Succeeded;
+    }
+
     public static IEnumerable<object[]> Visible_Set_TestData()
     {
         foreach (DialogResult dialogResult in Enum.GetValues(typeof(DialogResult)))