diff --git a/src/wine-host/editor.cpp b/src/wine-host/editor.cpp
index e7c9fdf8..788983ac 100644
--- a/src/wine-host/editor.cpp
+++ b/src/wine-host/editor.cpp
@@ -20,8 +20,6 @@
 
 #include <boost/container/small_vector.hpp>
 
-#include "xdnd-proxy.h"
-
 using namespace std::literals::chrono_literals;
 
 // A catchable alternative to `assert()`. Normally all of our `assert(!error)`
@@ -204,6 +202,7 @@ Editor::Editor(MainContext& main_context,
                std::optional<fu2::unique_function<void()>> timer_proc)
     : use_xembed(config.editor_xembed),
       x11_connection(xcb_connect(nullptr, nullptr), xcb_disconnect),
+      dnd_proxy_handle(WineXdndProxy::init_proxy()),
       client_area(get_maximum_screen_dimensions(*x11_connection)),
       // Create a window without any decoratiosn for easy embedding. The
       // combination of `WS_EX_TOOLWINDOW` and `WS_POPUP` causes the window to
diff --git a/src/wine-host/editor.h b/src/wine-host/editor.h
index cb2d0436..339ad803 100644
--- a/src/wine-host/editor.h
+++ b/src/wine-host/editor.h
@@ -31,6 +31,7 @@
 
 #include "../common/configuration.h"
 #include "utils.h"
+#include "xdnd-proxy.h"
 
 /**
  * The maximum number of Win32 messages to handle per message loop. This is
@@ -223,8 +224,17 @@ class Editor {
      */
     void do_xembed() const;
 
+    /**
+     * Every editor window gets its own X11 connection.
+     */
     std::shared_ptr<xcb_connection_t> x11_connection;
 
+    /**
+     * A handle for our Wine->X11 drag-and-drop proxy. We only have one of these
+     * per process, and it gets freed again when the last handle gets dropped.
+     */
+    WineXdndProxy::Handle dnd_proxy_handle;
+
     /**
      * The Wine window's client area, or the maximum size of that window. This
      * will be set to a size that's large enough to be able to enter full screen
diff --git a/src/wine-host/xdnd-proxy.cpp b/src/wine-host/xdnd-proxy.cpp
index 4336adc4..c32f67d7 100644
--- a/src/wine-host/xdnd-proxy.cpp
+++ b/src/wine-host/xdnd-proxy.cpp
@@ -16,6 +16,8 @@
 
 #include "xdnd-proxy.h"
 
+#include <atomic>
+
 // FIXME: Remove
 #include <iostream>
 
@@ -145,12 +147,34 @@ WineXdndProxy::WineXdndProxy()
                           WINEVENT_OUTOFCONTEXT | WINEVENT_SKIPOWNPROCESS),
           UnhookWinEvent) {}
 
-WineXdndProxy& WineXdndProxy::init_proxy() {
-    static std::unique_ptr<WineXdndProxy> instance;
-    if (!instance) {
-        // Protected constructors, hooray!
-        instance.reset(new WineXdndProxy{});
+/**
+ * The number of handles to our Wine->X11 drag-and-drop proxy object. To prevent
+ * running out of X11 connections when opening and closing a lot of plugin
+ * editors in a project, we'll free this again after the last editor in this
+ * process gets closed.
+ */
+static std::atomic_size_t instance_reference_count = 0;
+
+WineXdndProxy::Handle::Handle(WineXdndProxy& proxy) : proxy(proxy) {}
+
+WineXdndProxy::Handle::~Handle() noexcept {
+    if (instance_reference_count.fetch_sub(1) == 1) {
+        delete &proxy;
+    }
+}
+
+WineXdndProxy::Handle WineXdndProxy::init_proxy() {
+    // We're doing a bit of a hybrid between a COM-style reference counted smart
+    // pointer and a singleton here because we need to ensure that there's only
+    // one proxy per process, but we want to free up the X11 connection when
+    // it's not needed anymore. Because of that this pointer may point to
+    // deallocated memory, so the reference count should be leading here. Oh and
+    // explained elsewhere, we won't even bother making this thread safe because
+    // it can only be called from the GUI thread anyways.
+    static WineXdndProxy* instance = nullptr;
+    if (instance_reference_count.fetch_add(1) == 0) {
+        instance = new WineXdndProxy{};
     }
 
-    return *instance;
+    return Handle(*instance);
 }
diff --git a/src/wine-host/xdnd-proxy.h b/src/wine-host/xdnd-proxy.h
index d4ffbaab..ffbc3e0e 100644
--- a/src/wine-host/xdnd-proxy.h
+++ b/src/wine-host/xdnd-proxy.h
@@ -36,6 +36,35 @@ class WineXdndProxy {
     WineXdndProxy();
 
    public:
+    /**
+     * A sort of smart pointer for `WineXdndProxy`, similar to how the COM/VST3
+     * pointers work. We want to unregister the hooks and drop the X11
+     * connection when the last editor closes in a plugin group. This is not
+     * strictly necessary, but there's an open X11 client limit and otherwise
+     * opening and closing a bunch of editors would get you very close to that
+     * limit.
+     */
+    class Handle {
+       protected:
+        /**
+         * Before calling this, the reference count should be increased by one
+         * in `WineXdndProxy::init_proxy()`.
+         */
+        Handle(WineXdndProxy& proxy);
+
+       public:
+        /**
+         * Reduces the reference count by one, and frees `proxy` if this was the
+         * last handle.
+         */
+        ~Handle() noexcept;
+
+       private:
+        WineXdndProxy& proxy;
+
+        friend WineXdndProxy;
+    };
+
     /**
      * Initialize the Wine->X11 drag-and-drop proxy. Calling this will hook into
      * Wine's OLE drag and drop system by listening for the creation of special
@@ -47,8 +76,15 @@ class WineXdndProxy {
      * once from every plugin host instance. Because the actual data is stored
      * in a COM object, we can only handle drag-and-drop coming form this
      * process.
+     *
+     * This is sort of a singleton but not quite, as the `WineXdndProxy` is only
+     * alive for as long as there are open editors in this process. This is done
+     * to avoid opening too many X11 connections.
+     *
+     * @note This function, like everything other GUI realted, should be called
+     *   from the main thread that's running the Win32 message loop.
      */
-    static WineXdndProxy& init_proxy();
+    static WineXdndProxy::Handle init_proxy();
 
    private:
     std::unique_ptr<xcb_connection_t, decltype(&xcb_disconnect)> x11_connection;