diff --git a/src/client/Client.cpp b/src/client/Client.cpp
index 9679ca68c..b3589a1f0 100644
--- a/src/client/Client.cpp
+++ b/src/client/Client.cpp
@@ -131,7 +131,7 @@ void Client::Tick()
 			{
 				updateInfo = info.updateInfo;
 				applyUpdateInfo = true;
-				messageOfTheDay = info.messageOfTheDay;
+				SetMessageOfTheDay(info.messageOfTheDay);
 			}
 			for (auto &notification : info.notifications)
 			{
@@ -142,7 +142,7 @@ void Client::Tick()
 		{
 			if (!usingAltUpdateServer)
 			{
-				messageOfTheDay = ByteString::Build("Error while fetching MotD: ", ex.what()).FromUtf8();
+				SetMessageOfTheDay(ByteString::Build("Error while fetching MotD: ", ex.what()).FromUtf8());
 			}
 		}
 		versionCheckRequest.reset();
@@ -154,7 +154,7 @@ void Client::Tick()
 			auto info = alternateVersionCheckRequest->Finish();
 			updateInfo = info.updateInfo;
 			applyUpdateInfo = true;
-			messageOfTheDay = info.messageOfTheDay;
+			SetMessageOfTheDay(info.messageOfTheDay);
 			for (auto &notification : info.notifications)
 			{
 				AddServerNotification(notification);
@@ -162,7 +162,7 @@ void Client::Tick()
 		}
 		catch (const http::RequestError &ex)
 		{
-			messageOfTheDay = ByteString::Build("Error while checking for updates: ", ex.what()).FromUtf8();
+			SetMessageOfTheDay(ByteString::Build("Error while checking for updates: ", ex.what()).FromUtf8());
 		}
 		alternateVersionCheckRequest.reset();
 	}
diff --git a/src/client/http/requestmanager/Libcurl.cpp b/src/client/http/requestmanager/Libcurl.cpp
index 657b2085e..af8420fcb 100644
--- a/src/client/http/requestmanager/Libcurl.cpp
+++ b/src/client/http/requestmanager/Libcurl.cpp
@@ -296,13 +296,8 @@ namespace http
 		{
 			{
 				std::lock_guard lk(sharedStateMx);
-				for (auto &requestHandle : requestHandles)
-				{
-					if (requestHandle->statusCode)
-					{
-						requestHandlesToUnregister.push_back(requestHandle);
-					}
-				}
+				// Register new handles first. This always succeeds even if the handle is "failed early" so that
+				// a single MarkDone call could be issued on all handles further down in this block.
 				for (auto &requestHandle : requestHandlesToRegister)
 				{
 					// Must not be present
@@ -311,6 +306,17 @@ namespace http
 					RegisterRequestHandle(requestHandle);
 				}
 				requestHandlesToRegister.clear();
+				// Then unregister done handles. As explained above, registering a new handle may also immediately mark
+				// it done and we won't be coming back here until Wait() returns, so this has to come second.
+				for (auto &requestHandle : requestHandles)
+				{
+					if (requestHandle->statusCode)
+					{
+						requestHandlesToUnregister.push_back(requestHandle);
+					}
+				}
+				// Actually unregister handles queued to be unregistered. They can be queued just above, or from another thread.
+				// Thus, it's ok for them to be in the queue multiple times, but it's not ok to try to unregister them multiple times.
 				for (auto &requestHandle : requestHandlesToUnregister)
 				{
 					auto eraseFrom = std::remove(requestHandles.begin(), requestHandles.end(), requestHandle);