diff --git a/lib/server.js b/lib/server.js
index 0b81f4424..4cec6130e 100644
--- a/lib/server.js
+++ b/lib/server.js
@@ -1258,8 +1258,14 @@ Server.prototype._finishReqResCycle = function _finishReqResCycle(
         // after event has signature of function(req, res, route, err) {...}
         self.emit('after', req, res, route, err || res.err);
     } else {
-        // preserve error for actual finish
-        res.err = err;
+        // Store error for when the response is flushed and we actually emit the
+        // 'after' event. The "err" object passed to this method takes
+        // precedence, but in case it's not set, "res.err" may have been already
+        // set by another code path and we want to preserve it. The caveat thus
+        // is that the 'after' event will be emitted with the latest error that
+        // was set before the response is fully flushed. While not ideal, this
+        // is on purpose and accepted as a reasonable trade-off for now.
+        res.err = err || res.err;
     }
 };