diff --git a/include/maxscale/config_runtime.h b/include/maxscale/config_runtime.h
index 8384ebbb9..06ae263a8 100644
--- a/include/maxscale/config_runtime.h
+++ b/include/maxscale/config_runtime.h
@@ -144,3 +144,16 @@ bool runtime_create_listener(SERVICE *service, const char *name, const char *add
                              const char *auth_opt, const char *ssl_key,
                              const char *ssl_cert, const char *ssl_ca,
                              const char *ssl_version, const char *ssl_depth);
+
+/**
+ * @brief Destroy a listener
+ *
+ * This disables the listener by removing it from the polling system. It also
+ * removes any generated configurations for this listener.
+ *
+ * @param service Service where the listener exists
+ * @param name Name of the listener
+ *
+ * @return True if the listener was successfully destroyed
+ */
+bool runtime_destroy_listener(SERVICE *service, const char *name);
diff --git a/include/maxscale/service.h b/include/maxscale/service.h
index 723d1259d..caa773625 100644
--- a/include/maxscale/service.h
+++ b/include/maxscale/service.h
@@ -262,13 +262,13 @@ bool serviceStop(SERVICE *service);
 bool serviceStart(SERVICE *service);
 
 /**
- * @brief Start a listener for a service
+ * @brief Start new a listener for a service
  *
  * @param service Service where the listener is linked
  * @param port Listener to start
  * @return True if listener was started
  */
-bool serviceStartListener(SERVICE *service, SERV_LISTENER *port);
+bool serviceLaunchListener(SERVICE *service, SERV_LISTENER *port);
 
 /**
  * @brief Stop a listener for a service
diff --git a/server/core/config_runtime.c b/server/core/config_runtime.c
index f7d56628d..c5acb8fdd 100644
--- a/server/core/config_runtime.c
+++ b/server/core/config_runtime.c
@@ -412,9 +412,9 @@ bool runtime_create_listener(SERVICE *service, const char *name, const char *add
     {
         const char *print_addr = addr ? addr : "0.0.0.0";
         SERV_LISTENER *listener = serviceCreateListener(service, name, proto, addr,
-                                                     u_port, auth, auth_opt, ssl);
+                                                        u_port, auth, auth_opt, ssl);
 
-        if (listener && listener_serialize(listener) && serviceStartListener(service, listener))
+        if (listener && listener_serialize(listener) && serviceLaunchListener(service, listener))
         {
             MXS_NOTICE("Listener '%s' at %s:%s for service '%s' created",
                        name, print_addr, port, service->name);
@@ -429,3 +429,52 @@ bool runtime_create_listener(SERVICE *service, const char *name, const char *add
     spinlock_release(&crt_lock);
     return rval;
 }
+
+bool runtime_destroy_listener(SERVICE *service, const char *name)
+{
+    bool rval = false;
+    char filename[PATH_MAX];
+    snprintf(filename, sizeof(filename), "%s/%s.cnf", get_config_persistdir(), name);
+
+    spinlock_acquire(&crt_lock);
+
+    if (unlink(filename) == -1)
+    {
+        if (errno != ENOENT)
+        {
+            char err[MXS_STRERROR_BUFLEN];
+            MXS_ERROR("Failed to remove persisted listener configuration '%s': %d, %s",
+                      filename, errno, strerror_r(errno, err, sizeof(err)));
+        }
+        else
+        {
+            rval = false;
+            MXS_WARNING("Listener '%s' was not created at runtime. Remove the "
+                        "listener manually from the correct configuration file.",
+                        name);
+        }
+    }
+    else
+    {
+        rval = true;
+    }
+
+    if (rval)
+    {
+        rval = serviceStopListener(service, name);
+
+        if (rval)
+        {
+            MXS_NOTICE("Destroyed listener '%s' for service '%s'. The listener "
+                       "will be removed after the next restart of MaxScale.",
+                       name, service->name);
+        }
+        else
+        {
+            MXS_ERROR("Failed to destroy listener '%s' for service '%s'", name, service->name);
+        }
+    }
+
+    spinlock_release(&crt_lock);
+    return rval;
+}
diff --git a/server/core/service.c b/server/core/service.c
index 128f018f8..3df2e19af 100644
--- a/server/core/service.c
+++ b/server/core/service.c
@@ -490,7 +490,7 @@ int serviceInitialize(SERVICE *service)
     return listeners;
 }
 
-bool serviceStartListener(SERVICE *service, SERV_LISTENER *port)
+bool serviceLaunchListener(SERVICE *service, SERV_LISTENER *port)
 {
     return serviceStartPort(service, port);
 }
diff --git a/server/modules/routing/debugcli/debugcmd.c b/server/modules/routing/debugcli/debugcmd.c
index 34907326c..fb584b268 100644
--- a/server/modules/routing/debugcli/debugcmd.c
+++ b/server/modules/routing/debugcli/debugcmd.c
@@ -1111,6 +1111,18 @@ static void destroyServer(DCB *dcb, SERVER *server)
     }
 }
 
+static void destroyListener(DCB *dcb, SERVICE *service, const char *name)
+{
+    if (runtime_destroy_listener(service, name))
+    {
+        dcb_printf(dcb, "Destroyed listener '%s'\n", name);
+    }
+    else
+    {
+        dcb_printf(dcb, "Failed to destroy listener '%s', see log file for more details\n", name);
+    }
+}
+
 struct subcommand destroyoptions[] =
 {
     {
@@ -1119,6 +1131,12 @@ struct subcommand destroyoptions[] =
         "Usage: destroy server NAME",
         {ARG_TYPE_SERVER}
     },
+    {
+        "listener", 2, 2, destroyListener,
+        "Destroy a listener",
+        "Usage: destroy listener SERVICE NAME",
+        {ARG_TYPE_SERVICE, ARG_TYPE_STRING}
+    },
     {
         EMPTY_OPTION
     }