diff --git a/mitogen/core.py b/mitogen/core.py
index 5b1d5298..3d2fc288 100644
--- a/mitogen/core.py
+++ b/mitogen/core.py
@@ -2087,6 +2087,8 @@ class Router(object):
         self._last_handle = itertools.count(1000)
         #: handle -> (persistent?, func(msg))
         self._handle_map = {}
+        #: Context -> set { handle, .. }
+        self._handles_by_respondent = {}
         self.add_handler(self._on_del_route, DEL_ROUTE)
 
     def __repr__(self):
@@ -2117,7 +2119,7 @@ class Router(object):
 
     def _on_broker_exit(self):
         while self._handle_map:
-            _, (_, func, _) = self._handle_map.popitem()
+            _, (_, func, _, _) = self._handle_map.popitem()
             func(Message.dead())
 
     def context_by_id(self, context_id, via_id=None, create=True, name=None):
@@ -2151,8 +2153,8 @@ class Router(object):
         `dst_id`. If a specific route for `dst_id` is not known, a reference to
         the parent context's stream is returned.
         """
-        return self._stream_by_id.get(dst_id,
-            self._stream_by_id.get(mitogen.parent_id))
+        parent = self._stream_by_id.get(mitogen.parent_id)
+        return self._stream_by_id.get(dst_id, parent)
 
     def del_handler(self, handle):
         """
@@ -2161,7 +2163,9 @@ class Router(object):
         :raises KeyError:
             The handle wasn't registered.
         """
-        del self._handle_map[handle]
+        _, _, _, respondent = self._handle_map.pop(handle)
+        if respondent:
+            self._handles_by_respondent[respondent].discard(handle)
 
     def add_handler(self, fn, handle=None, persist=True,
                     policy=None, respondent=None):
@@ -2216,19 +2220,22 @@ class Router(object):
         handle = handle or next(self._last_handle)
         _vv and IOLOG.debug('%r.add_handler(%r, %r, %r)', self, fn, handle, persist)
 
+        self._handle_map[handle] = persist, fn, policy, respondent
         if respondent:
-            assert policy is None
-            def policy(msg, _stream):
-                return msg.is_dead or msg.src_id == respondent.context_id
-            def on_disconnect():
-                if handle in self._handle_map:
-                    fn(Message.dead())
-                    del self._handle_map[handle]
-            listen(respondent, 'disconnect', on_disconnect)
+            if respondent not in self._handles_by_respondent:
+                self._handles_by_respondent[respondent] = set()
+                listen(respondent, 'disconnect',
+                       lambda: self._on_respondent_disconnect(respondent))
+            self._handles_by_respondent[respondent].add(handle)
 
-        self._handle_map[handle] = persist, fn, policy
         return handle
 
+    def _on_respondent_disconnect(self, context):
+        for handle in self._handles_by_respondent.pop(context, ()):
+            _, fn, _, _  = self._handle_map[handle]
+            fn(Message.dead())
+            del self._handle_map[handle]
+
     def on_shutdown(self, broker):
         """Called during :meth:`Broker.shutdown`, informs callbacks registered
         with :meth:`add_handle_cb` the connection is dead."""
@@ -2238,16 +2245,25 @@ class Router(object):
             _v and LOG.debug('%r.on_shutdown(): killing %r: %r', self, handle, fn)
             fn(Message.dead())
 
+    def _maybe_send_dead(self, msg):
+        if msg.reply_to and not msg.is_dead:
+            msg.reply(Message.dead(), router=self)
+
     refused_msg = 'Refused by policy.'
 
     def _invoke(self, msg, stream):
         # IOLOG.debug('%r._invoke(%r)', self, msg)
         try:
-            persist, fn, policy = self._handle_map[msg.handle]
+            persist, fn, policy, respondent = self._handle_map[msg.handle]
         except KeyError:
             LOG.error('%r: invalid handle: %r', self, msg)
-            if msg.reply_to and not msg.is_dead:
-                msg.reply(Message.dead())
+            self._maybe_send_dead(msg)
+            return
+
+        if respondent and not (msg.is_dead or
+                               msg.src_id == respondent.context_id):
+            LOG.error('%r: reply from unexpected context: %r', self, msg)
+            self._maybe_send_dead(msg)
             return
 
         if policy and not policy(msg, stream):
@@ -2261,17 +2277,13 @@ class Router(object):
             return
 
         if not persist:
-            del self._handle_map[msg.handle]
+            self.del_handler(msg.handle)
 
         try:
             fn(msg)
         except Exception:
             LOG.exception('%r._invoke(%r): %r crashed', self, msg, fn)
 
-    def _maybe_send_dead(self, msg):
-        if msg.reply_to and not msg.is_dead:
-            msg.reply(Message.dead(), router=self)
-
     def _async_route(self, msg, in_stream=None):
         """
         Arrange for `msg` to be forwarded towards its destination. If its