diff --git a/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker.cpp b/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker.cpp
index b29e838ff..91a984dea 100644
--- a/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker.cpp
+++ b/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker.cpp
@@ -136,6 +136,10 @@ QNetworkReply *CardPictureLoaderWorker::makeRequest(const QUrl &url, CardPicture
 
 void CardPictureLoaderWorker::resetRequestQuota()
 {
+    // Allowances are seeded per host on demand in processSingleRequest(), so a
+    // rate-limited host never gets a fresh full quota mid-second.
+    hostQuotaRemaining.clear();
+
     QDateTime now = QDateTime::currentDateTime();
     for (auto it = hostRequestQuota.begin(); it != hostRequestQuota.end(); ++it) {
         if (!hostLast429.contains(it.key()) || now.msecsTo(hostLast429.value(it.key())) < -QUOTA_RECOVER_MS) {
@@ -143,11 +147,6 @@ void CardPictureLoaderWorker::resetRequestQuota()
         }
     }
 
-    for (const auto &request : requestLoadQueue) {
-        const QString host = request.first.host();
-        hostQuotaRemaining.insert(host, hostRequestQuota.value(host, MAX_REQUESTS_PER_SEC));
-    }
-
     processQueuedRequests();
 }
 
@@ -188,10 +187,20 @@ void CardPictureLoaderWorker::dispatchQueuedRequest()
 
 bool CardPictureLoaderWorker::processSingleRequest()
 {
+    QDateTime now = QDateTime::currentDateTime();
     for (int i = 0; i < requestLoadQueue.size(); ++i) {
         const auto &request = requestLoadQueue.at(i);
-        QString host = request.first.host();
-        int allowance = hostQuotaRemaining.value(host, MAX_REQUESTS_PER_SEC);
+        const QString host = request.first.host();
+        // Don't dispatch requests to a host that is currently in its 429 backoff.
+        if (CardPictureLoaderWorkerWork::rateLimiter().isRateLimited(host, now)) {
+            continue;
+        }
+        // Seed the allowance only now, so a host that was rate limited last second
+        // doesn't get a fresh full quota the moment it is queried mid-second.
+        if (!hostQuotaRemaining.contains(host)) {
+            hostQuotaRemaining.insert(host, hostRequestQuota.value(host, MAX_REQUESTS_PER_SEC));
+        }
+        int allowance = hostQuotaRemaining.value(host);
         if (allowance > 0) {
             hostQuotaRemaining.insert(host, allowance - 1);
             makeRequest(request.first, request.second);
diff --git a/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.cpp b/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.cpp
index 66c56337c..072a919d7 100644
--- a/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.cpp
+++ b/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.cpp
@@ -22,6 +22,11 @@ static const QStringList MD5_BLACKLIST = {
     "fbc7d763c08771c260b39e2115414eeb"  // Current card back hash
 };
 
+ServerRateLimiter &CardPictureLoaderWorkerWork::rateLimiter()
+{
+    return s_rateLimiter;
+}
+
 CardPictureLoaderWorkerWork::CardPictureLoaderWorkerWork(const CardPictureLoaderWorker *worker, const ExactCard &toLoad)
     : QObject(nullptr), cardToDownload(CardPictureToLoad(toLoad)),
       picDownload(SettingsCache::instance().downloads().getPicDownload())
diff --git a/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.h b/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.h
index 1e56a4373..8490cb3ac 100644
--- a/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.h
+++ b/cockatrice/src/interface/card_picture_loader/card_picture_loader_worker_work.h
@@ -43,6 +43,9 @@ public:
 
     CardPictureToLoad cardToDownload; ///< The card and associated URLs to try downloading
 
+    /** @brief Shared per-server 429 backoff state. */
+    static ServerRateLimiter &rateLimiter();
+
 public slots:
     /**
      * @brief Handles a finished network reply for the card image.