diff --git a/src/windows/wslc/services/ContainerService.cpp b/src/windows/wslc/services/ContainerService.cpp
index ed248a0f1..9d39c5174 100644
--- a/src/windows/wslc/services/ContainerService.cpp
+++ b/src/windows/wslc/services/ContainerService.cpp
@@ -287,7 +287,6 @@ int ContainerService::Run(Session& session, const std::string& image, ContainerO
 {
     // Create the container
     auto runningContainer = CreateInternal(session, image, runOptions);
-    runningContainer.SetDeleteOnClose(false);
     auto& container = runningContainer.Get();
 
     // Start the created container
@@ -295,6 +294,9 @@ int ContainerService::Run(Session& session, const std::string& image, ContainerO
     WI_SetFlagIf(startFlags, WSLCContainerStartFlagsAttach, !runOptions.Detach);
     THROW_IF_FAILED(container.Start(startFlags, nullptr)); // TODO: Error message, detach keys
 
+    // Disable auto-delete only after successful start
+    runningContainer.SetDeleteOnClose(false);
+
     // Handle attach if requested
     if (WI_IsFlagSet(startFlags, WSLCContainerStartFlagsAttach))
     {
diff --git a/src/windows/wslcsession/WSLCContainer.cpp b/src/windows/wslcsession/WSLCContainer.cpp
index 35d3000a0..9ea93e496 100644
--- a/src/windows/wslcsession/WSLCContainer.cpp
+++ b/src/windows/wslcsession/WSLCContainer.cpp
@@ -1274,12 +1274,10 @@ std::unique_ptr<WSLCContainerImpl> WSLCContainerImpl::Open(
         {
             auto allocation = virtualMachine.TryAllocatePort(e.VmPort, e.Family, e.Protocol);
 
-            THROW_HR_IF_MSG(
+            THROW_HR_WITH_USER_ERROR_IF(
                 HRESULT_FROM_WIN32(ERROR_ALREADY_EXISTS),
-                !allocation,
-                "Port %hu is in use, cannot open container %hs",
-                e.VmPort,
-                dockerContainer.Id.c_str());
+                std::format(L"Port {} is already in use, cannot open container {}", e.VmPort, dockerContainer.Id),
+                !allocation);
 
             inserted.VmMapping.AssignVmPort(allocation);
         }
@@ -1443,12 +1441,10 @@ void WSLCContainerImpl::MapPorts()
                 auto allocatedPort =
                     m_virtualMachine.TryAllocatePort(e.ContainerPort, e.VmMapping.BindAddress.si_family, e.VmMapping.Protocol);
 
-                THROW_HR_IF_MSG(
+                THROW_HR_WITH_USER_ERROR_IF(
                     HRESULT_FROM_WIN32(ERROR_ALREADY_EXISTS),
-                    !allocatedPort,
-                    "Port %hu is in use, cannot start container %hs",
-                    e.ContainerPort,
-                    m_id.c_str());
+                    std::format(L"Port {} is already in use, cannot start container {}", e.VmMapping.HostPort(), m_id),
+                    !allocatedPort);
 
                 e.VmMapping.AssignVmPort(allocatedPort);
 
@@ -1456,7 +1452,20 @@ void WSLCContainerImpl::MapPorts()
             }
         }
 
-        m_virtualMachine.MapPort(e.VmMapping);
+        try
+        {
+            m_virtualMachine.MapPort(e.VmMapping);
+        }
+        catch (const wil::ResultException& ex)
+        {
+            if (ex.GetErrorCode() == HRESULT_FROM_WIN32(ERROR_ALREADY_EXISTS) || ex.GetErrorCode() == HRESULT_FROM_WIN32(WSAEADDRINUSE))
+            {
+                THROW_HR_WITH_USER_ERROR(
+                    HRESULT_FROM_WIN32(ERROR_ALREADY_EXISTS),
+                    std::format(L"Port {} is already in use, cannot start container {}", e.VmMapping.HostPort(), m_id));
+            }
+            throw;
+        }
     }
 }
 
diff --git a/test/windows/wslc/e2e/WSLCE2EContainerCreateTests.cpp b/test/windows/wslc/e2e/WSLCE2EContainerCreateTests.cpp
index d1cc2e2ea..e6bfdcff7 100644
--- a/test/windows/wslc/e2e/WSLCE2EContainerCreateTests.cpp
+++ b/test/windows/wslc/e2e/WSLCE2EContainerCreateTests.cpp
@@ -988,8 +988,6 @@ class WSLCE2EContainerCreateTests
     TEST_METHOD(WSLCE2E_Container_Run_PortAlreadyInUse)
     {
         // Bug: https://github.com/microsoft/WSL/issues/14448
-        SKIP_TEST_NOT_IMPL();
-
         WSL2_TEST_ONLY();
 
         // Start a container with a simple server listening on a port
@@ -1002,9 +1000,16 @@ class WSLCE2EContainerCreateTests
             GetPythonHttpServerScript(ContainerTestPort)));
         result1.Verify({.Stderr = L"", .ExitCode = 0});
 
+        auto containersBefore = ListAllContainers().size();
+
         // Attempt to start another container mapping the same host port
         auto result2 = RunWslc(std::format(L"container run -p {}:{} {}", HostTestPort1, ContainerTestPort, DebianImage.NameAndTag()));
         result2.Verify({.ExitCode = 1});
+        VERIFY_IS_TRUE(result2.Stderr.has_value() && result2.Stderr.value().find(L"is already in use") != std::wstring::npos);
+
+        // Verify the failed container was not left behind
+        auto containersAfter = ListAllContainers().size();
+        VERIFY_ARE_EQUAL(containersBefore, containersAfter);
     }
 
     // https://github.com/microsoft/WSL/issues/14433