diff --git a/macos/Sources/Features/Terminal/TerminalController.swift b/macos/Sources/Features/Terminal/TerminalController.swift
index 7070a4867..5fd346583 100644
--- a/macos/Sources/Features/Terminal/TerminalController.swift
+++ b/macos/Sources/Features/Terminal/TerminalController.swift
@@ -1278,6 +1278,13 @@ class TerminalController: BaseTerminalController, TabGroupCloseCoordinator.Contr
 
         // Whenever we resize save our last position and size for the next start.
         LastWindowPosition.shared.save(window)
+
+        if let window = self.window as? TerminalWindow {
+            // Expand the title frame to new width.
+            // This is needed because when the new window size becomes bigger,
+            // window's title will be clipped again.
+            window.syncWindowTitleAppearance()
+        }
     }
 
     func windowDidBecomeMain(_ notification: Notification) {
diff --git a/macos/Sources/Features/Terminal/Window Styles/TerminalWindow.swift b/macos/Sources/Features/Terminal/Window Styles/TerminalWindow.swift
index 737d146f1..81b6666a1 100644
--- a/macos/Sources/Features/Terminal/Window Styles/TerminalWindow.swift	
+++ b/macos/Sources/Features/Terminal/Window Styles/TerminalWindow.swift	
@@ -1,4 +1,5 @@
 import AppKit
+import Combine
 import SwiftUI
 import GhosttyKit
 
@@ -277,12 +278,6 @@ class TerminalWindow: NSWindow {
     /// added.
     static let tabBarIdentifier: NSUserInterfaceItemIdentifier = .init("_ghosttyTabBar")
 
-    var hasMoreThanOneTabs: Bool {
-        /// accessing ``tabGroup?.windows`` here
-        /// will cause other edge cases, be careful
-        (tabbedWindows?.count ?? 0) > 1
-    }
-
     func isTabBar(_ childViewController: NSTitlebarAccessoryViewController) -> Bool {
         if childViewController.identifier == nil {
             // The good case
@@ -396,12 +391,9 @@ class TerminalWindow: NSWindow {
             // Whenever we change the window title we must also update our
             // tab title if we're using custom fonts.
             tab.attributedTitle = attributedTitle
-            /// We also needs to update this here, just in case
-            /// the value is not what we want
-            ///
-            /// Check ``titlebarFont`` down below
-            /// to see why we need to check `hasMoreThanOneTabs` here
-            titlebarTextField?.usesSingleLineMode = !hasMoreThanOneTabs
+            guard title != oldValue else { return }
+
+            syncWindowTitleAppearance()
         }
     }
 
@@ -409,25 +401,28 @@ class TerminalWindow: NSWindow {
     var titlebarFont: NSFont? {
         didSet {
             let font = titlebarFont ?? NSFont.titleBarFont(ofSize: NSFont.systemFontSize)
-
-            titlebarTextField?.font = font
-            /// We check `hasMoreThanOneTabs` here because the system
-            /// may copy this setting to the tab’s text field at some point(e.g. entering/exiting fullscreen),
-            /// which can cause the title to be vertically misaligned (shifted downward).
-            ///
-            /// This behaviour is the opposite of what happens in the title bar’s text field, which is quite odd...
-            titlebarTextField?.usesSingleLineMode = !hasMoreThanOneTabs
             tab.attributedTitle = attributedTitle
+
+            // We need to call this every time the font is set,
+            // after entering or exiting fullscreen, or other cases,
+            // AppKit will reset the font.
+            syncWindowTitleAppearance(font: font)
         }
     }
 
-    // Find the NSTextField responsible for displaying the titlebar's title.
-    private var titlebarTextField: NSTextField? {
-        titlebarContainer?
+    // Find the array of NSTextField responsible for displaying the titlebar's title.
+    // In fullscreen mode, there'll be two of them.
+    private var titlebarTextFields: [NSTextField] {
+        (titlebarContainer?
             .firstDescendant(withClassName: "NSTitlebarView")?
-            .firstDescendant(withClassName: "NSTextField") as? NSTextField
+            .descendants(withClassName: "NSTextField")
+            .compactMap { $0 as? NSTextField } ?? [])
+            .filter({ $0.superview?.className == "NSTitlebarView" })
     }
 
+    // Cancellables for the frame change of the text fields in the titlebar.
+    private var titlebarTextFieldFrameCancellables = Set<AnyCancellable>()
+
     // Return a styled representation of our title property.
     var attributedTitle: NSAttributedString? {
         guard let titlebarFont = titlebarFont else { return nil }
@@ -463,6 +458,65 @@ class TerminalWindow: NSWindow {
 
     // MARK: Positioning And Styling
 
+    /// Update titlebarTextField's size and font
+    func syncWindowTitleAppearance(font: NSFont? = nil) {
+        titlebarTextFields.forEach { field in
+            if let font {
+                field.font = font
+            }
+        }
+
+        titlebarTextFieldFrameCancellables.removeAll()
+
+        // macOS 15 doesn't seem to need to adjust the frame.
+        //
+        // When using custom font, we always expand the frame to
+        // show the text properly.
+        //
+        // AppKit will relayout the frame when the font changes, that's
+        // why we need this hack in the first place.
+        guard #available(macOS 26.0, *), titlebarFont != nil else {
+            return
+        }
+
+        titlebarTextFields.forEach { field in
+            setWindowTitleFrameSize(field)
+        }
+
+        // We need to observe changes to make the frame correct in some cases:
+        //
+        // 1. Entering fullscreen mode.
+        //    > Updating the frame when it's hidden doesn't seem to work.
+        // 2. Exiting fullscreen mode.
+        // 3. Resizing the window.
+        // 3. Maybe more...
+
+        titlebarTextFields.forEach { field in
+            field.postsFrameChangedNotifications = true
+            NotificationCenter.default
+                .publisher(for: NSView.frameDidChangeNotification, object: field)
+                .compactMap { $0.object as? NSTextField }
+                .sink { [weak self] in
+                    self?.setWindowTitleFrameSize($0)
+                }
+                .store(in: &titlebarTextFieldFrameCancellables)
+        }
+    }
+
+    private func setWindowTitleFrameSize(_ textfield: NSTextField) {
+        guard let superview = textfield.superview else { return }
+
+        // Button group size estimate: 92.
+        // Make the available space a little bit smaller.
+        let fittingSize = textfield.sizeThatFits(superview.bounds.insetBy(dx: 92/2 + 6, dy: 0).size)
+        // We make the frame a little bit higher so fixed-width fonts can
+        // align center vertically as well.
+        let properSize = CGSize(width: fittingSize.width, height: fittingSize.height * 1.1)
+
+        guard textfield.frame.size != properSize else { return }
+        textfield.frame.size = properSize
+    }
+
     /// This is called by the controller when there is a need to reset the window appearance.
     func syncAppearance(_ surfaceConfig: Ghostty.SurfaceView.DerivedConfig) {
         // If our window is not visible, then we do nothing. Some things such as blurring