diff --git a/src/cascadia/TerminalApp/TabHeaderControl.h b/src/cascadia/TerminalApp/TabHeaderControl.h
index 39744b2bcb0a..41c81fb783d3 100644
--- a/src/cascadia/TerminalApp/TabHeaderControl.h
+++ b/src/cascadia/TerminalApp/TabHeaderControl.h
@@ -23,6 +23,7 @@ namespace winrt::TerminalApp::implementation
         WINRT_CALLBACK(PropertyChanged, Windows::UI::Xaml::Data::PropertyChangedEventHandler);
         OBSERVABLE_GETSET_PROPERTY(winrt::hstring, Title, _PropertyChangedHandlers);
         OBSERVABLE_GETSET_PROPERTY(bool, IsPaneZoomed, _PropertyChangedHandlers);
+        OBSERVABLE_GETSET_PROPERTY(double, RenamerMaxWidth, _PropertyChangedHandlers);
         OBSERVABLE_GETSET_PROPERTY(bool, IsProgressRingActive, _PropertyChangedHandlers);
         OBSERVABLE_GETSET_PROPERTY(bool, IsProgressRingIndeterminate, _PropertyChangedHandlers);
         OBSERVABLE_GETSET_PROPERTY(uint32_t, ProgressValue, _PropertyChangedHandlers);
diff --git a/src/cascadia/TerminalApp/TabHeaderControl.idl b/src/cascadia/TerminalApp/TabHeaderControl.idl
index 0fc8fc2da3ee..808b72067c4a 100644
--- a/src/cascadia/TerminalApp/TabHeaderControl.idl
+++ b/src/cascadia/TerminalApp/TabHeaderControl.idl
@@ -9,6 +9,7 @@ namespace TerminalApp
     {
         String Title { get; set; };
         Boolean IsPaneZoomed { get; set; };
+        Double RenamerMaxWidth { get; set; };
         Boolean IsProgressRingActive { get; set; };
         Boolean IsProgressRingIndeterminate { get; set; };
         UInt32 ProgressValue { get; set; };
diff --git a/src/cascadia/TerminalApp/TabHeaderControl.xaml b/src/cascadia/TerminalApp/TabHeaderControl.xaml
index 65e8b5ee7b96..ba8350d3b123 100644
--- a/src/cascadia/TerminalApp/TabHeaderControl.xaml
+++ b/src/cascadia/TerminalApp/TabHeaderControl.xaml
@@ -9,8 +9,25 @@ the MIT License. See LICENSE in the project root for license information. -->
     xmlns:mux="using:Microsoft.UI.Xaml.Controls"
     xmlns:d="http://schemas.microsoft.com/expression/blend/2008"
     xmlns:mc="http://schemas.openxmlformats.org/markup-compatibility/2006"
-    mc:Ignorable="d">
+    mc:Ignorable="d"
+    MinHeight="16">
 
+    <UserControl.Resources>
+        <ResourceDictionary>
+            <ResourceDictionary.ThemeDictionaries>
+                <ResourceDictionary x:Key="Light">
+                    <Thickness x:Key="TextControlBorderThemeThicknessFocused">0,0,0,1</Thickness>
+                </ResourceDictionary>
+                <ResourceDictionary x:Key="Dark">
+                    <Thickness x:Key="TextControlBorderThemeThicknessFocused">0,0,0,1</Thickness>
+                </ResourceDictionary>
+                <ResourceDictionary x:Key="HighContrast">
+                    <Thickness x:Key="TextControlBorderThemeThicknessFocused">0,0,0,1</Thickness>
+                </ResourceDictionary>
+            </ResourceDictionary.ThemeDictionaries>
+        </ResourceDictionary>
+    </UserControl.Resources>
+    
     <StackPanel x:Name="HeaderStackPanel"
                 Orientation="Horizontal">
         <mux:ProgressRing x:Name="HeaderProgressRing"
@@ -39,8 +56,11 @@ the MIT License. See LICENSE in the project root for license information. -->
                  Visibility="Collapsed"
                  MinHeight="0"
                  Padding="4,0,4,0"
-                 Margin="0,-8,0,-8"
                  MaxLength="1024"
-                 LostFocus="RenameBoxLostFocusHandler"/>
+                 LostFocus="RenameBoxLostFocusHandler"
+                 Height="16"
+                 FontSize="12"
+                 IsSpellCheckEnabled="False"
+                 MaxWidth="{x:Bind RenamerMaxWidth, Mode=OneWay}"/>
     </StackPanel>
 </UserControl>
diff --git a/src/cascadia/TerminalApp/TerminalTab.cpp b/src/cascadia/TerminalApp/TerminalTab.cpp
index 3777f0ab19ee..8e7252c4e41d 100644
--- a/src/cascadia/TerminalApp/TerminalTab.cpp
+++ b/src/cascadia/TerminalApp/TerminalTab.cpp
@@ -50,6 +50,9 @@ namespace winrt::TerminalApp::implementation
                 tab->SetTabText(title);
             }
         });
+
+        _UpdateHeaderControlMaxWidth();
+
         // Use our header control as the TabViewItem's header
         TabViewItem().Header(_headerControl);
     }
@@ -75,6 +78,26 @@ namespace winrt::TerminalApp::implementation
         _RecalculateAndApplyTabColor();
     }
 
+    winrt::fire_and_forget TerminalTab::_UpdateHeaderControlMaxWidth()
+    {
+        auto weakThis{ get_weak() };
+
+        co_await winrt::resume_foreground(TabViewItem().Dispatcher());
+
+        if (auto tab{ weakThis.get() })
+        {
+            const auto settings{ winrt::TerminalApp::implementation::AppLogic::CurrentAppSettings() };
+            if (settings.GlobalSettings().TabWidthMode() == winrt::Microsoft::UI::Xaml::Controls::TabViewWidthMode::SizeToContent)
+            {
+                tab->_headerControl.RenamerMaxWidth(HeaderRenameBoxWidthTitleLength);
+            }
+            else
+            {
+                tab->_headerControl.RenamerMaxWidth(HeaderRenameBoxWidthDefault);
+            }
+        }
+    }
+
     void TerminalTab::_SetToolTip(const winrt::hstring& tabTitle)
     {
         WUX::Controls::ToolTip toolTip{};
@@ -169,6 +192,9 @@ namespace winrt::TerminalApp::implementation
     void TerminalTab::UpdateSettings(const winrt::TerminalApp::TerminalSettings& settings, const GUID& profile)
     {
         _rootPane->UpdateSettings(settings, profile);
+
+        // The tabWidthMode may have changed, update the header control accordingly
+        _UpdateHeaderControlMaxWidth();
     }
 
     // Method Description:
diff --git a/src/cascadia/TerminalApp/TerminalTab.h b/src/cascadia/TerminalApp/TerminalTab.h
index 1ae7ad2e6dd9..62783d5160e4 100644
--- a/src/cascadia/TerminalApp/TerminalTab.h
+++ b/src/cascadia/TerminalApp/TerminalTab.h
@@ -7,6 +7,9 @@
 #include "TabBase.h"
 #include "TerminalTab.g.h"
 
+static constexpr double HeaderRenameBoxWidthDefault{ 165 };
+static constexpr double HeaderRenameBoxWidthTitleLength{ std::numeric_limits<double>::infinity() };
+
 // fwdecl unittest classes
 namespace TerminalAppLocalTests
 {
@@ -102,6 +105,7 @@ namespace winrt::TerminalApp::implementation
 
         void _MakeTabViewItem();
 
+        winrt::fire_and_forget _UpdateHeaderControlMaxWidth();
         void _SetToolTip(const winrt::hstring& tabTitle);
 
         void _CreateContextMenu() override;