diff --git a/src/cascadia/TerminalApp/Pane.cpp b/src/cascadia/TerminalApp/Pane.cpp
index fe3607b4678..73054081cc7 100644
--- a/src/cascadia/TerminalApp/Pane.cpp
+++ b/src/cascadia/TerminalApp/Pane.cpp
@@ -1340,6 +1340,29 @@ TermControl Pane::GetLastFocusedTerminalControl()
     }
 }
 
+IPaneContent Pane::GetLastFocusedContent()
+{
+    if (!_IsLeaf())
+    {
+        if (_lastActive)
+        {
+            auto pane = shared_from_this();
+            while (const auto p = pane->_parentChildPath.lock())
+            {
+                if (p->_IsLeaf())
+                {
+                    return p->_content;
+                }
+                pane = p;
+            }
+            // We didn't find our child somehow, they might have closed under us.
+        }
+        return _firstChild->GetLastFocusedContent();
+    }
+
+    return _content;
+}
+
 // Method Description:
 // - Gets the TermControl of this pane. If this Pane is not a leaf this will
 //   return the nullptr;
@@ -1480,7 +1503,11 @@ void Pane::UpdateVisuals()
 void Pane::_Focus()
 {
     _GotFocusHandlers(shared_from_this(), FocusState::Programmatic);
-    _content.Focus(FocusState::Programmatic);
+    if (const auto& lastContent{ GetLastFocusedContent() })
+    {
+        lastContent.Focus(FocusState::Programmatic);
+    }
+    
 }
 
 // Method Description:
@@ -2176,7 +2203,7 @@ void Pane::_SetupEntranceAnimation()
         auto child = isFirstChild ? _firstChild : _secondChild;
         auto childGrid = child->_root;
         // If we are splitting a parent pane this may be null
-        auto control = child->_content.GetRoot();
+        auto control = child->_content ? child->_content.GetRoot() : nullptr;
         // Build up our animation:
         // * it'll take as long as our duration (200ms)
         // * it'll change the value of our property from 0 to secondSize
diff --git a/src/cascadia/TerminalApp/Pane.h b/src/cascadia/TerminalApp/Pane.h
index e8631047f36..f096ae5c9ab 100644
--- a/src/cascadia/TerminalApp/Pane.h
+++ b/src/cascadia/TerminalApp/Pane.h
@@ -73,6 +73,7 @@ class Pane : public std::enable_shared_from_this<Pane>
 
     std::shared_ptr<Pane> GetActivePane();
     winrt::Microsoft::Terminal::Control::TermControl GetLastFocusedTerminalControl();
+    winrt::TerminalApp::IPaneContent GetLastFocusedContent();
     winrt::Microsoft::Terminal::Control::TermControl GetTerminalControl() const;
     winrt::Microsoft::Terminal::Settings::Model::Profile GetFocusedProfile();
     bool IsConnectionClosed() const;
diff --git a/src/cascadia/TerminalApp/TerminalPage.cpp b/src/cascadia/TerminalApp/TerminalPage.cpp
index 8e271850844..1ef15cafe68 100644
--- a/src/cascadia/TerminalApp/TerminalPage.cpp
+++ b/src/cascadia/TerminalApp/TerminalPage.cpp
@@ -4598,7 +4598,10 @@ namespace winrt::TerminalApp::implementation
         {
             if (const auto& pane{ tab->GetActivePane() })
             {
-                terminalBrush = pane->GetContent().BackgroundBrush();
+                if (const auto& lastContent{ pane->GetLastFocusedContent() })
+                {
+                    terminalBrush = lastContent.BackgroundBrush();
+                }
             }
         }