diff --git a/src/cascadia/TerminalApp/TerminalPage.cpp b/src/cascadia/TerminalApp/TerminalPage.cpp
index 12cec3594..cba5ea4a9 100644
--- a/src/cascadia/TerminalApp/TerminalPage.cpp
+++ b/src/cascadia/TerminalApp/TerminalPage.cpp
@@ -457,6 +457,11 @@ namespace winrt::TerminalApp::implementation
                     co_return;
                 }
             }
+
+            // GH#6586: now that we're done processing all startup commands,
+            // focus the active control. This will work as expected for both
+            // commandline invocations and for `wt` action invocations.
+            _GetActiveControl().Focus(FocusState::Programmatic);
         }
         if (initial)
         {
@@ -1414,6 +1419,14 @@ namespace winrt::TerminalApp::implementation
             _UnZoomIfNeeded();
 
             tab.SplitPane(realSplitType, splitSize, profile, newControl);
+
+            // After GH#6586, the control will no longer focus itself
+            // automatically when it's finished being laid out. Manually focus
+            // the control here instead.
+            if (_startupState == StartupState::Initialized)
+            {
+                _GetActiveControl().Focus(FocusState::Programmatic);
+            }
         }
         CATCH_LOG();
     }
diff --git a/src/cascadia/TerminalControl/TermControl.cpp b/src/cascadia/TerminalControl/TermControl.cpp
index aaa562c34..e36fadd6a 100644
--- a/src/cascadia/TerminalControl/TermControl.cpp
+++ b/src/cascadia/TerminalControl/TermControl.cpp
@@ -681,8 +681,11 @@ namespace winrt::Microsoft::Terminal::Control::implementation
             DispatcherTimer cursorTimer;
             cursorTimer.Interval(std::chrono::milliseconds(blinkTime));
             cursorTimer.Tick({ get_weak(), &TermControl::_CursorTimerTick });
-            cursorTimer.Start();
             _cursorTimer.emplace(std::move(cursorTimer));
+            // As of GH#6586, don't start the cursor timer immediately, and
+            // don't show the cursor initially. We'll show the cursor and start
+            // the timer when the control is first focused. cursorTimer.Start();
+            _core.CursorOn(false);
         }
         else
         {
@@ -711,12 +714,6 @@ namespace winrt::Microsoft::Terminal::Control::implementation
         // Now that the renderer is set up, update the appearance for initialization
         _UpdateAppearanceFromUIThread(_settings);
 
-        // Focus the control here. If we do it during control initialization, then
-        //      focus won't actually get passed to us. I believe this is because
-        //      we're not technically a part of the UI tree yet, so focusing us
-        //      becomes a no-op.
-        this->Focus(FocusState::Programmatic);
-
         _initializedTerminal = true;
 
         // MSFT 33353327: If the AutomationPeer was created before we were done initializing,