diff --git a/src/cascadia/Remoting/Monarch.cpp b/src/cascadia/Remoting/Monarch.cpp
index 9cec5917d..f1b13480a 100644
--- a/src/cascadia/Remoting/Monarch.cpp
+++ b/src/cascadia/Remoting/Monarch.cpp
@@ -147,6 +147,7 @@ namespace winrt::Microsoft::Terminal::Remoting::implementation
     // - <none>
     void Monarch::SignalClose(const uint64_t peasantId)
     {
+        _clearOldMruEntries(peasantId);
         _peasants.erase(peasantId);
         _WindowClosedHandlers(nullptr, nullptr);
     }
diff --git a/src/cascadia/UnitTests_Remoting/RemotingTests.cpp b/src/cascadia/UnitTests_Remoting/RemotingTests.cpp
index 5480bc609..2d5131460 100644
--- a/src/cascadia/UnitTests_Remoting/RemotingTests.cpp
+++ b/src/cascadia/UnitTests_Remoting/RemotingTests.cpp
@@ -140,11 +140,16 @@ namespace RemotingUnitTests
 
         TEST_METHOD(TestSummonMostRecentIsQuake);
 
+        TEST_METHOD(TestSummonAfterWindowClose);
+
         TEST_CLASS_SETUP(ClassSetup)
         {
             return true;
         }
 
+        static void _closePeasant(const com_ptr<Remoting::implementation::Monarch>& m,
+                                  const uint64_t peasantID);
+
         static void _killPeasant(const com_ptr<Remoting::implementation::Monarch>& m,
                                  const uint64_t peasantID);
 
@@ -164,6 +169,19 @@ namespace RemotingUnitTests
         }
     };
 
+    // Helper to tell the monarch that a peasant is closing, this emulates when
+    // a peasant is closed normally instead of when it crashes.
+    void RemotingTests::_closePeasant(const com_ptr<Remoting::implementation::Monarch>& m,
+                                      const uint64_t peasantID)
+    {
+        if (peasantID <= 0)
+        {
+            return;
+        }
+
+        m->SignalClose(peasantID);
+    }
+
     // Helper to replace the specified peasant in a monarch with a
     // "DeadPeasant", which will emulate what happens when the peasant process
     // dies.
@@ -2378,4 +2396,127 @@ namespace RemotingUnitTests
         }
     }
 
+    void RemotingTests::TestSummonAfterWindowClose()
+    {
+        Log::Comment(L"Test that we can summon a window on the current desktop,"
+                     L" when the MRU window on that desktop closes normally.");
+
+        const winrt::guid guid1{ Utils::GuidFromString(L"{11111111-1111-1111-1111-111111111111}") };
+        const winrt::guid guid2{ Utils::GuidFromString(L"{22222222-2222-2222-2222-222222222222}") };
+
+        constexpr auto monarch0PID = 12345u;
+        constexpr auto peasant1PID = 23456u;
+        constexpr auto peasant2PID = 34567u;
+        constexpr auto peasant3PID = 45678u;
+
+        auto m0 = make_private<Remoting::implementation::Monarch>(monarch0PID);
+        auto p1 = make_private<Remoting::implementation::Peasant>(peasant1PID);
+        auto p2 = make_private<Remoting::implementation::Peasant>(peasant2PID);
+        auto p3 = make_private<Remoting::implementation::Peasant>(peasant3PID);
+
+        p1->WindowName(L"one");
+        p2->WindowName(L"two");
+        p3->WindowName(L"three");
+
+        VERIFY_ARE_EQUAL(0, p1->GetID());
+        VERIFY_ARE_EQUAL(0, p2->GetID());
+        VERIFY_ARE_EQUAL(0, p3->GetID());
+
+        m0->AddPeasant(*p1);
+        m0->AddPeasant(*p2);
+        m0->AddPeasant(*p3);
+
+        VERIFY_ARE_EQUAL(1, p1->GetID());
+        VERIFY_ARE_EQUAL(2, p2->GetID());
+        VERIFY_ARE_EQUAL(3, p3->GetID());
+
+        VERIFY_ARE_EQUAL(3u, m0->_peasants.size());
+
+        bool p1ExpectedToBeSummoned = false;
+        bool p2ExpectedToBeSummoned = false;
+        bool p3ExpectedToBeSummoned = false;
+
+        p1->SummonRequested([&](auto&&, auto&&) {
+            Log::Comment(L"p1 summoned");
+            VERIFY_IS_TRUE(p1ExpectedToBeSummoned);
+        });
+        p2->SummonRequested([&](auto&&, auto&&) {
+            Log::Comment(L"p2 summoned");
+            VERIFY_IS_TRUE(p2ExpectedToBeSummoned);
+        });
+        p3->SummonRequested([&](auto&&, auto&&) {
+            Log::Comment(L"p3 summoned");
+            VERIFY_IS_TRUE(p3ExpectedToBeSummoned);
+        });
+
+        {
+            Log::Comment(L"Activate the first peasant, first desktop");
+            Remoting::WindowActivatedArgs activatedArgs{ p1->GetID(),
+                                                         p1->GetPID(), // USE PID as HWND, because these values don't _really_ matter
+                                                         guid1,
+                                                         winrt::clock().now() };
+            p1->ActivateWindow(activatedArgs);
+        }
+        {
+            Log::Comment(L"Activate the second peasant, second desktop");
+            Remoting::WindowActivatedArgs activatedArgs{ p2->GetID(),
+                                                         p2->GetPID(), // USE PID as HWND, because these values don't _really_ matter
+                                                         guid2,
+                                                         winrt::clock().now() };
+            p2->ActivateWindow(activatedArgs);
+        }
+        {
+            Log::Comment(L"Activate the third peasant, first desktop");
+            Remoting::WindowActivatedArgs activatedArgs{ p3->GetID(),
+                                                         p3->GetPID(), // USE PID as HWND, because these values don't _really_ matter
+                                                         guid1,
+                                                         winrt::clock().now() };
+            p3->ActivateWindow(activatedArgs);
+        }
+
+        Log::Comment(L"Create a mock IVirtualDesktopManager to handle checking if a window is on a given desktop");
+        auto manager = winrt::make_self<MockDesktopManager>();
+        m0->_desktopManager = manager.try_as<IVirtualDesktopManager>();
+
+        auto firstCallback = [&](HWND h, BOOL* result) -> HRESULT {
+            Log::Comment(L"firstCallback: Checking if window is on desktop 1");
+
+            const uint64_t hwnd = reinterpret_cast<uint64_t>(h);
+            if (hwnd == peasant1PID || hwnd == peasant3PID)
+            {
+                *result = true;
+            }
+            else if (hwnd == peasant2PID)
+            {
+                *result = false;
+            }
+            else
+            {
+                VERIFY_IS_TRUE(false, L"IsWindowOnCurrentVirtualDesktop called with unexpected value");
+            }
+            return S_OK;
+        };
+        manager->pfnIsWindowOnCurrentVirtualDesktop = firstCallback;
+
+        Remoting::SummonWindowSelectionArgs args;
+
+        Log::Comment(L"Summon window three - it is the MRU on desktop 1");
+        p3ExpectedToBeSummoned = true;
+        args.OnCurrentDesktop(true);
+        m0->SummonWindow(args);
+        VERIFY_IS_TRUE(args.FoundMatch());
+
+        Log::Comment(L"Close window 3. Window 1 is now the MRU on desktop 1.");
+        RemotingTests::_closePeasant(m0, p3->GetID());
+
+        Log::Comment(L"Summon window three - it is the MRU on desktop 1");
+        p1ExpectedToBeSummoned = true;
+        p2ExpectedToBeSummoned = false;
+        p3ExpectedToBeSummoned = false;
+        args.FoundMatch(false);
+        args.OnCurrentDesktop(true);
+        m0->SummonWindow(args);
+        VERIFY_IS_TRUE(args.FoundMatch());
+    }
+
 }