diff --git a/CHANGELOG.md b/CHANGELOG.md
index 1b5fcd7117e..64db8227437 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -32,6 +32,7 @@ BUG FIXES:
    [[GH-4234](https://github.com/hashicorp/nomad/issues/4234)]
  * driver/docker: Fix docker credential helper support [[GH-4266](https://github.com/hashicorp/nomad/issues/4266)]
  * driver/docker: Fix panic when docker client configuration options are invalid [[GH-4303](https://github.com/hashicorp/nomad/issues/4303)]
+ * rpc: Fix RPC tunneling when running both client/server on one machine [[GH-4317](https://github.com/hashicorp/nomad/issues/4317)]
 
 ## 0.8.3 (April 27, 2018)
 
diff --git a/command/agent/agent.go b/command/agent/agent.go
index 2eddcad021c..34453a04d7e 100644
--- a/command/agent/agent.go
+++ b/command/agent/agent.go
@@ -314,9 +314,24 @@ func (a *Agent) clientConfig() (*clientconfig.Config, error) {
 	if conf == nil {
 		conf = clientconfig.DefaultConfig()
 	}
+
+	// If we are running a server, append both its bind and advertise address so
+	// we are able to at least talk to the local server even if that isn't
+	// configured explicitly. This handles both running server and client on one
+	// host and -dev mode.
+	conf.Servers = a.config.Client.Servers
 	if a.server != nil {
-		conf.RPCHandler = a.server
+		if a.config.AdvertiseAddrs == nil || a.config.AdvertiseAddrs.RPC == "" {
+			return nil, fmt.Errorf("AdvertiseAddrs is nil or empty")
+		} else if a.config.normalizedAddrs == nil || a.config.normalizedAddrs.RPC == "" {
+			return nil, fmt.Errorf("normalizedAddrs is nil or empty")
+		}
+
+		conf.Servers = append(conf.Servers,
+			a.config.normalizedAddrs.RPC,
+			a.config.AdvertiseAddrs.RPC)
 	}
+
 	conf.LogOutput = a.logOutput
 	conf.LogLevel = a.config.LogLevel
 	conf.DevMode = a.config.DevMode
@@ -333,7 +348,6 @@ func (a *Agent) clientConfig() (*clientconfig.Config, error) {
 	if a.config.Client.AllocDir != "" {
 		conf.AllocDir = a.config.Client.AllocDir
 	}
-	conf.Servers = a.config.Client.Servers
 	if a.config.Client.NetworkInterface != "" {
 		conf.NetworkInterface = a.config.Client.NetworkInterface
 	}
diff --git a/command/agent/agent_test.go b/command/agent/agent_test.go
index 2926231239c..89c556808e6 100644
--- a/command/agent/agent_test.go
+++ b/command/agent/agent_test.go
@@ -9,7 +9,9 @@ import (
 	"testing"
 	"time"
 
+	cstructs "github.com/hashicorp/nomad/client/structs"
 	"github.com/hashicorp/nomad/helper"
+	"github.com/hashicorp/nomad/nomad/structs"
 	sconfig "github.com/hashicorp/nomad/nomad/structs/config"
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
@@ -1057,3 +1059,24 @@ func TestServer_ShouldReload_ShouldHandleMultipleChanges(t *testing.T) {
 		require.False(shouldReloadRPC)
 	}
 }
+
+func TestAgent_ProxyRPC_Dev(t *testing.T) {
+	t.Parallel()
+	agent := NewTestAgent(t, t.Name(), nil)
+	defer agent.Shutdown()
+
+	id := agent.client.NodeID()
+	req := &structs.NodeSpecificRequest{
+		NodeID: id,
+		QueryOptions: structs.QueryOptions{
+			Region: agent.server.Region(),
+		},
+	}
+
+	time.Sleep(100 * time.Millisecond)
+
+	var resp cstructs.ClientStatsResponse
+	if err := agent.RPC("ClientStats.Stats", req, &resp); err != nil {
+		t.Fatalf("err: %v", err)
+	}
+}
diff --git a/nomad/client_rpc.go b/nomad/client_rpc.go
index 5a3498de7bf..1493348ebd3 100644
--- a/nomad/client_rpc.go
+++ b/nomad/client_rpc.go
@@ -31,6 +31,9 @@ func (s *Server) getNodeConn(nodeID string) (*nodeConnState, bool) {
 	s.nodeConnsLock.RLock()
 	defer s.nodeConnsLock.RUnlock()
 	conns, ok := s.nodeConns[nodeID]
+	if !ok {
+		return nil, false
+	}
 
 	// Return the latest conn
 	var state *nodeConnState