diff --git a/server/client.go b/server/client.go
index ba0ce263..7ff1c4e2 100644
--- a/server/client.go
+++ b/server/client.go
@@ -435,6 +435,7 @@ type clientOpts struct {
 	Protocol    int    `json:"protocol"`
 	Account     string `json:"account,omitempty"`
 	AccountNew  bool   `json:"new_account,omitempty"`
+	Headers     bool   `json:"headers,omitempty"`
 
 	// Routes only
 	Import *SubjectPermission `json:"import,omitempty"`
@@ -1414,6 +1415,9 @@ func (c *client) processConnect(arg []byte) error {
 	account := c.opts.Account
 	accountNew := c.opts.AccountNew
 	ujwt := c.opts.JWT
+	// For headers both need to support. If the server supports headers
+	/// it will have been set to true before this is called.
+	c.headers = c.headers && c.opts.Headers
 	c.mu.Unlock()
 
 	if srv != nil {
@@ -1845,6 +1849,10 @@ func (c *client) processPong() {
 
 // Header pubs take form HPUB <subject> [reply] <hdr_len> <total_len>\r\n
 func (c *client) processHeaderPub(arg []byte) error {
+	if !c.headers {
+		return ErrMsgHeadersNotSupported
+	}
+
 	// Unroll splitArgs to avoid runtime/heap issues
 	a := [MAX_HPUB_ARGS][]byte{}
 	args := a[:0]
diff --git a/server/client_test.go b/server/client_test.go
index 9e78bc11..91594f6e 100644
--- a/server/client_test.go
+++ b/server/client_test.go
@@ -195,6 +195,7 @@ func TestServerHeaderSupport(t *testing.T) {
 	opts := defaultServerOptions
 	opts.Port = -1
 	s := New(&opts)
+
 	c, _, l := newClientForServer(s)
 	defer c.close()
 
@@ -212,6 +213,7 @@ func TestServerHeaderSupport(t *testing.T) {
 	opts.NoHeaderSupport = true
 	opts.Port = -1
 	s = New(&opts)
+
 	c, _, l = newClientForServer(s)
 	defer c.close()
 
@@ -223,6 +225,43 @@ func TestServerHeaderSupport(t *testing.T) {
 	}
 }
 
+// This test specifically is not testing how headers are encoded in a raw msg.
+// It wants to make sure the serve and clients agreement on when to use headers
+// is bi-directional and functions properly.
+func TestClientHeaderSupport(t *testing.T) {
+	opts := defaultServerOptions
+	opts.Port = -1
+	s := New(&opts)
+
+	c, _, _ := newClientForServer(s)
+	defer c.close()
+
+	// Even though the server supports headers we need to explicitly say we do in the
+	// CONNECT. If we do not we should get an error.
+	if err := c.parse([]byte("CONNECT {}\r\nHPUB foo 0 2\r\nok\r\n")); err != ErrMsgHeadersNotSupported {
+		t.Fatalf("Expected to receive an error, got %v", err)
+	}
+
+	// This should succeed.
+	c, _, _ = newClientForServer(s)
+	defer c.close()
+
+	if err := c.parse([]byte("CONNECT {\"headers\":true}\r\nHPUB foo 0 2\r\nok\r\n")); err != nil {
+		t.Fatalf("Unexpected error %v", err)
+	}
+
+	// Now start a server without support.
+	opts.NoHeaderSupport = true
+	opts.Port = -1
+	s = New(&opts)
+
+	c, _, _ = newClientForServer(s)
+	defer c.close()
+	if err := c.parse([]byte("CONNECT {\"headers\":true}\r\nHPUB foo 0 2\r\nok\r\n")); err != ErrMsgHeadersNotSupported {
+		t.Fatalf("Expected to receive an error, got %v", err)
+	}
+}
+
 func TestNonTLSConnectionState(t *testing.T) {
 	_, c, _ := setupClient()
 	defer c.close()
diff --git a/server/parser_test.go b/server/parser_test.go
index 945f514d..7afd269d 100644
--- a/server/parser_test.go
+++ b/server/parser_test.go
@@ -299,6 +299,7 @@ func TestParsePubBadSize(t *testing.T) {
 
 func TestParseHeaderPub(t *testing.T) {
 	c := dummyClient()
+	c.headers = true
 
 	hpub := []byte("HPUB foo 12 17\r\nname:derek\r\nHELLO\r")
 	if err := c.parse(hpub); err != nil || c.state != MSG_END_N {
@@ -360,6 +361,7 @@ func TestParseHeaderPub(t *testing.T) {
 
 func TestParseHeaderPubArg(t *testing.T) {
 	c := dummyClient()
+	c.headers = true
 
 	for _, test := range []struct {
 		arg     string