diff --git a/src/httpserver.cpp b/src/httpserver.cpp
index a5d56be0fb6..ad6d020d3a3 100644
--- a/src/httpserver.cpp
+++ b/src/httpserver.cpp
@@ -1072,6 +1072,9 @@ void HTTPRequest::WriteReply(HTTPStatusCode status, std::span<const std::byte> r
         // in the next loop iteration.
         m_client->m_send_ready = true;
     }
+
+    // Signal to the I/O loop that we are ready to handle the next request.
+    m_client->m_req_busy = false;
 }
 
 util::Expected<void, std::string> HTTPServer::BindAndStartListening(const CService& to)
@@ -1293,10 +1296,13 @@ void HTTPServer::SocketHandlerConnected(const IOReadiness& io_readiness) const
                     client->m_recv_buffer.end(),
                     buf,
                     buf + nrecv);
-                // Process as much received data as we can
-                MaybeDispatchRequestsFromClient(client);
             }
         }
+        // Process as much received data as we can.
+        // This executes for every client whether or not reading or writing
+        // took place because it also (might) parse a request we have already
+        // received and pass it to a worker thread.
+        MaybeDispatchRequestsFromClient(client);
     }
 }
 
@@ -1410,8 +1416,20 @@ void HTTPServer::MaybeDispatchRequestsFromClient(const std::shared_ptr<HTTPRemot
             client->m_origin,
             client->m_id);
 
-        // handle request
-        m_request_dispatcher(std::move(req));
+        // add request to client queue
+        client->m_req_queue.push_back(std::move(req));
+    }
+
+    // If we are already handling a request from
+    // this client, do nothing. We'll check again on the next I/O
+    // loop iteration.
+    if (client->m_req_busy) return;
+
+    // Otherwise, if there is a pending request in the queue, handle it.
+    if (!client->m_req_queue.empty()) {
+        client->m_req_busy = true;
+        m_request_dispatcher(std::move(client->m_req_queue.front()));
+        client->m_req_queue.pop_front();
     }
 }
 
diff --git a/src/httpserver.h b/src/httpserver.h
index cbb9dd43298..339cd45f222 100644
--- a/src/httpserver.h
+++ b/src/httpserver.h
@@ -6,6 +6,7 @@
 #define BITCOIN_HTTPSERVER_H
 
 #include <atomic>
+#include <deque>
 #include <functional>
 #include <memory>
 #include <optional>
@@ -538,6 +539,16 @@ public:
      */
     std::vector<std::byte> m_recv_buffer{};
 
+    //! Requests from a client must be processed in the order in which
+    //! they were received, blocking on a per-client basis. We won't
+    //! process the next request in the queue if we are currently busy
+    //! handling a previous request.
+    std::deque<std::unique_ptr<HTTPRequest>> m_req_queue;
+
+    //! Set to true by the I/O thread when a request is popped off
+    //! and passed to a worker thread, reset to false by the worker thread.
+    std::atomic_bool m_req_busy{false};
+
     /**
      * Response data destined for this client.
      * Written to by http worker threads, read and erased by HTTPServer I/O thread