diff --git a/cmd/influxd/config.go b/cmd/influxd/config.go
index edb7362d05..d94426b999 100644
--- a/cmd/influxd/config.go
+++ b/cmd/influxd/config.go
@@ -218,8 +218,6 @@ func NewConfig() *Config {
 	c := &Config{}
 	c.Port = DefaultClusterPort
 
-	c.HTTPAPI.Port = DefaultClusterPort
-
 	c.Data.Enabled = DefaultDataEnabled
 	c.Broker.Enabled = DefaultBrokerEnabled
 
@@ -278,11 +276,18 @@ func NewTestConfig() (*Config, error) {
 
 // APIAddr returns the TCP binding address for the API server.
 func (c *Config) APIAddr() string {
+	// Default to cluster bind address if not overriden
 	ba := c.BindAddress
 	if c.HTTPAPI.BindAddress != "" {
 		ba = c.HTTPAPI.BindAddress
 	}
-	return net.JoinHostPort(ba, strconv.Itoa(c.HTTPAPI.Port))
+
+	// Default to cluster port if not overridden
+	bp := c.Port
+	if c.HTTPAPI.Port != 0 {
+		bp = c.HTTPAPI.Port
+	}
+	return net.JoinHostPort(ba, strconv.Itoa(bp))
 }
 
 // APIAddrUDP returns the UDP address for the series listener.
diff --git a/cmd/influxd/run.go b/cmd/influxd/run.go
index de75676765..a1dc8c2ef5 100644
--- a/cmd/influxd/run.go
+++ b/cmd/influxd/run.go
@@ -47,6 +47,7 @@ type Node struct {
 
 	adminServer     *admin.Server
 	clusterListener net.Listener // The cluster TCP listener
+	apiListener     net.Listener // The API TCP listener
 }
 
 func (s *Node) Close() error {
@@ -54,6 +55,10 @@ func (s *Node) Close() error {
 		return err
 	}
 
+	if err := s.closeAPIListener(); err != nil {
+		return err
+	}
+
 	if err := s.closeAdminServer(); err != nil {
 		return err
 	}
@@ -92,16 +97,14 @@ func (s *Node) closeAdminServer() error {
 	return nil
 }
 
-func (s *Node) openClusterListener(addr string, h http.Handler) error {
+func (s *Node) openListener(desc, addr string, h http.Handler) (net.Listener, error) {
 	var err error
-	// We want to make sure we are spun up before we exit this function, so we manually listen and serve
 	listener, err := net.Listen("tcp", addr)
 	if err != nil {
-		return err
+		return nil, err
 	}
-	s.clusterListener = listener
 	go func() {
-		err := http.Serve(s.clusterListener, h)
+		err := http.Serve(listener, h)
 
 		// The listener was closed so exit
 		// See https://github.com/golang/go/issues/4373
@@ -109,9 +112,37 @@ func (s *Node) openClusterListener(addr string, h http.Handler) error {
 			return
 		}
 		if err != nil {
-			log.Fatalf("TCP server failed to server on %s: %s", addr, err)
+			log.Fatalf("%s server failed to serve on %s: %s", desc, addr, err)
 		}
 	}()
+	return listener, nil
+
+}
+
+func (s *Node) openAPIListener(addr string, h http.Handler) error {
+	var err error
+	s.apiListener, err = s.openListener("API", addr, h)
+	if err != nil {
+		return err
+	}
+	return nil
+}
+
+func (s *Node) closeAPIListener() error {
+	var err error
+	if s.apiListener != nil {
+		err = s.apiListener.Close()
+		s.apiListener = nil
+	}
+	return err
+}
+
+func (s *Node) openClusterListener(addr string, h http.Handler) error {
+	var err error
+	s.clusterListener, err = s.openListener("Cluster", addr, h)
+	if err != nil {
+		return err
+	}
 	return nil
 }
 
@@ -227,9 +258,9 @@ func (cmd *RunCommand) Open(config *Config, join string) *Node {
 
 	err := cmd.node.openClusterListener(cmd.config.ClusterAddr(), h)
 	if err != nil {
-		log.Fatalf("TCP server failed to listen on %s. %s ", cmd.config.ClusterAddr(), err)
+		log.Fatalf("Cluster server failed to listen on %s. %s ", cmd.config.ClusterAddr(), err)
 	}
-	log.Printf("TCP server listening on %s", cmd.config.ClusterAddr())
+	log.Printf("Cluster server listening on %s", cmd.config.ClusterAddr())
 
 	var s *influxdb.Server
 	// Open server, initialize or join as necessary.
@@ -389,6 +420,14 @@ func (cmd *RunCommand) Open(config *Config, join string) *Node {
 		}
 	}
 
+	if cmd.config.APIAddr() != cmd.config.ClusterAddr() {
+		err := cmd.node.openAPIListener(cmd.config.APIAddr(), h)
+		if err != nil {
+			log.Fatalf("API server failed to listen on %s. %s ", cmd.config.APIAddr(), err)
+		}
+	}
+	log.Printf("API server listening on %s", cmd.config.APIAddr())
+
 	return cmd.node
 }