diff --git a/agent/acl_endpoint.go b/agent/acl_endpoint.go
index c30f5f55ef..9a40a6596c 100644
--- a/agent/acl_endpoint.go
+++ b/agent/acl_endpoint.go
@@ -14,16 +14,24 @@ type aclCreateResponse struct {
 	ID string
 }
 
-// ACLDisabled handles if ACL datacenter is not configured
-func ACLDisabled(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+// checkACLDisabled will return a standard response if ACLs are disabled. This
+// returns true if they are disabled and we should not continue.
+func (s *HTTPServer) checkACLDisabled(resp http.ResponseWriter, req *http.Request) bool {
+	if s.agent.config.ACLDatacenter != "" {
+		return false
+	}
+
 	resp.WriteHeader(http.StatusUnauthorized)
 	fmt.Fprint(resp, "ACL support disabled")
-	return nil, nil
+	return true
 }
 
 // ACLBootstrap is used to perform a one-time ACL bootstrap operation on
 // a cluster to get the first management token.
 func (s *HTTPServer) ACLBootstrap(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "PUT" {
 		return nil, MethodNotAllowedError{req.Method, []string{"PUT"}}
 	}
@@ -48,6 +56,9 @@ func (s *HTTPServer) ACLBootstrap(resp http.ResponseWriter, req *http.Request) (
 }
 
 func (s *HTTPServer) ACLDestroy(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "PUT" {
 		return nil, MethodNotAllowedError{req.Method, []string{"PUT"}}
 	}
@@ -74,6 +85,9 @@ func (s *HTTPServer) ACLDestroy(resp http.ResponseWriter, req *http.Request) (in
 }
 
 func (s *HTTPServer) ACLCreate(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "PUT" {
 		return nil, MethodNotAllowedError{req.Method, []string{"PUT"}}
 	}
@@ -81,6 +95,9 @@ func (s *HTTPServer) ACLCreate(resp http.ResponseWriter, req *http.Request) (int
 }
 
 func (s *HTTPServer) ACLUpdate(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "PUT" {
 		return nil, MethodNotAllowedError{req.Method, []string{"PUT"}}
 	}
@@ -129,6 +146,9 @@ func (s *HTTPServer) aclSet(resp http.ResponseWriter, req *http.Request, update
 }
 
 func (s *HTTPServer) ACLClone(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "PUT" {
 		return nil, MethodNotAllowedError{req.Method, []string{"PUT"}}
 	}
@@ -181,6 +201,9 @@ func (s *HTTPServer) ACLClone(resp http.ResponseWriter, req *http.Request) (inte
 }
 
 func (s *HTTPServer) ACLGet(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "GET" {
 		return nil, MethodNotAllowedError{req.Method, []string{"GET"}}
 	}
@@ -215,6 +238,9 @@ func (s *HTTPServer) ACLGet(resp http.ResponseWriter, req *http.Request) (interf
 }
 
 func (s *HTTPServer) ACLList(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "GET" {
 		return nil, MethodNotAllowedError{req.Method, []string{"GET"}}
 	}
@@ -241,6 +267,9 @@ func (s *HTTPServer) ACLList(resp http.ResponseWriter, req *http.Request) (inter
 }
 
 func (s *HTTPServer) ACLReplicationStatus(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "GET" {
 		return nil, MethodNotAllowedError{req.Method, []string{"GET"}}
 	}
diff --git a/agent/acl_endpoint_test.go b/agent/acl_endpoint_test.go
index 9aba5154c3..aa15c48686 100644
--- a/agent/acl_endpoint_test.go
+++ b/agent/acl_endpoint_test.go
@@ -3,14 +3,53 @@ package agent
 import (
 	"bytes"
 	"encoding/json"
+	"fmt"
 	"net/http"
 	"net/http/httptest"
+	"strings"
 	"testing"
 
 	"github.com/hashicorp/consul/acl"
 	"github.com/hashicorp/consul/agent/structs"
 )
 
+func TestACL_Disabled_Response(t *testing.T) {
+	t.Parallel()
+	a := NewTestAgent(t.Name(), "")
+	defer a.Shutdown()
+
+	tests := []func(resp http.ResponseWriter, req *http.Request) (interface{}, error){
+		a.srv.ACLBootstrap,
+		a.srv.ACLDestroy,
+		a.srv.ACLCreate,
+		a.srv.ACLUpdate,
+		a.srv.ACLClone,
+		a.srv.ACLGet,
+		a.srv.ACLList,
+		a.srv.ACLReplicationStatus,
+		a.srv.AgentToken, // See TestAgent_Token.
+	}
+	for i, tt := range tests {
+		t.Run(fmt.Sprintf("%d", i), func(t *testing.T) {
+			req, _ := http.NewRequest("PUT", "/should/not/care", nil)
+			resp := httptest.NewRecorder()
+			obj, err := tt(resp, req)
+			if err != nil {
+				t.Fatalf("err: %v", err)
+			}
+			if obj != nil {
+				t.Fatalf("bad: %#v", obj)
+			}
+			if got, want := resp.Code, http.StatusUnauthorized; got != want {
+				t.Fatalf("got %d want %d", got, want)
+			}
+			if !strings.Contains(resp.Body.String(), "ACL support disabled") {
+				t.Fatalf("bad: %#v", resp)
+			}
+		})
+	}
+}
+
 func makeTestACL(t *testing.T, srv *HTTPServer) string {
 	body := bytes.NewBuffer(nil)
 	enc := json.NewEncoder(body)
diff --git a/agent/agent_endpoint.go b/agent/agent_endpoint.go
index bf74827234..39b38294dd 100644
--- a/agent/agent_endpoint.go
+++ b/agent/agent_endpoint.go
@@ -809,6 +809,9 @@ func (h *httpLogHandler) HandleLog(log string) {
 }
 
 func (s *HTTPServer) AgentToken(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+	if s.checkACLDisabled(resp, req) {
+		return nil, nil
+	}
 	if req.Method != "PUT" {
 		return nil, MethodNotAllowedError{req.Method, []string{"PUT"}}
 	}
diff --git a/agent/agent_endpoint_test.go b/agent/agent_endpoint_test.go
index 3426b3bac1..427154f9e1 100644
--- a/agent/agent_endpoint_test.go
+++ b/agent/agent_endpoint_test.go
@@ -1771,6 +1771,10 @@ func TestAgent_Monitor_ACLDeny(t *testing.T) {
 
 func TestAgent_Token(t *testing.T) {
 	t.Parallel()
+
+	// The behavior of this handler when ACLs are disabled is vetted over
+	// in TestACL_Disabled_Response since there's already good infra set
+	// up over there to test this, and it calls the common function.
 	a := NewTestAgent(t.Name(), TestACLConfig()+`
 		acl_token = ""
 		acl_agent_token = ""
diff --git a/agent/http.go b/agent/http.go
index a51e2c944d..ca3085fd42 100644
--- a/agent/http.go
+++ b/agent/http.go
@@ -77,27 +77,15 @@ func (s *HTTPServer) handler(enableDebug bool) http.Handler {
 	mux.HandleFunc("/", s.Index)
 
 	// API V1.
-	if s.agent.config.ACLDatacenter != "" {
-		handleFuncMetrics("/v1/acl/bootstrap", s.wrap(s.ACLBootstrap))
-		handleFuncMetrics("/v1/acl/create", s.wrap(s.ACLCreate))
-		handleFuncMetrics("/v1/acl/update", s.wrap(s.ACLUpdate))
-		handleFuncMetrics("/v1/acl/destroy/", s.wrap(s.ACLDestroy))
-		handleFuncMetrics("/v1/acl/info/", s.wrap(s.ACLGet))
-		handleFuncMetrics("/v1/acl/clone/", s.wrap(s.ACLClone))
-		handleFuncMetrics("/v1/acl/list", s.wrap(s.ACLList))
-		handleFuncMetrics("/v1/acl/replication", s.wrap(s.ACLReplicationStatus))
-		handleFuncMetrics("/v1/agent/token/", s.wrap(s.AgentToken))
-	} else {
-		handleFuncMetrics("/v1/acl/bootstrap", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/acl/create", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/acl/update", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/acl/destroy/", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/acl/info/", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/acl/clone/", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/acl/list", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/acl/replication", s.wrap(ACLDisabled))
-		handleFuncMetrics("/v1/agent/token/", s.wrap(ACLDisabled))
-	}
+	handleFuncMetrics("/v1/acl/bootstrap", s.wrap(s.ACLBootstrap))
+	handleFuncMetrics("/v1/acl/create", s.wrap(s.ACLCreate))
+	handleFuncMetrics("/v1/acl/update", s.wrap(s.ACLUpdate))
+	handleFuncMetrics("/v1/acl/destroy/", s.wrap(s.ACLDestroy))
+	handleFuncMetrics("/v1/acl/info/", s.wrap(s.ACLGet))
+	handleFuncMetrics("/v1/acl/clone/", s.wrap(s.ACLClone))
+	handleFuncMetrics("/v1/acl/list", s.wrap(s.ACLList))
+	handleFuncMetrics("/v1/acl/replication", s.wrap(s.ACLReplicationStatus))
+	handleFuncMetrics("/v1/agent/token/", s.wrap(s.AgentToken))
 	handleFuncMetrics("/v1/agent/self", s.wrap(s.AgentSelf))
 	handleFuncMetrics("/v1/agent/maintenance", s.wrap(s.AgentNodeMaintenance))
 	handleFuncMetrics("/v1/agent/reload", s.wrap(s.AgentReload))