diff --git a/server/config_check_test.go b/server/config_check_test.go
index 94e0afbe..21582afd 100644
--- a/server/config_check_test.go
+++ b/server/config_check_test.go
@@ -1464,6 +1464,16 @@ func TestConfigCheck(t *testing.T) {
 			errorLine: 6,
 			errorPos:  10,
 		},
+		{
+			name: "ambiguous store dir",
+			config: `
+                                store_dir: "foo"
+                                jetstream {
+                                  store_dir: "bar"
+                                }
+                        `,
+			err: fmt.Errorf(`Duplicate 'store_dir' configuration`),
+		},
 	}
 
 	checkConfig := func(config string) error {
@@ -1499,10 +1509,17 @@ func TestConfigCheck(t *testing.T) {
 			}
 
 			if err != nil && expectedErr != nil {
-				msg := fmt.Sprintf("%s:%d:%d: %s", conf, test.errorLine, test.errorPos, expectedErr.Error())
-				if test.reason != "" {
-					msg += ": " + test.reason
+				var msg string
+
+				if test.errorPos > 0 {
+					msg = fmt.Sprintf("%s:%d:%d: %s", conf, test.errorLine, test.errorPos, expectedErr.Error())
+					if test.reason != "" {
+						msg += ": " + test.reason
+					}
+				} else {
+					msg = test.reason
 				}
+
 				if !strings.Contains(err.Error(), msg) {
 					t.Errorf("Expected:\n%q\ngot:\n%q", msg, err.Error())
 				}
diff --git a/server/ocsp.go b/server/ocsp.go
index 6c1c9091..a4556f0b 100644
--- a/server/ocsp.go
+++ b/server/ocsp.go
@@ -14,6 +14,7 @@
 package server
 
 import (
+	"crypto/sha256"
 	"crypto/tls"
 	"crypto/x509"
 	"encoding/asn1"
@@ -22,6 +23,8 @@ import (
 	"fmt"
 	"io/ioutil"
 	"net/http"
+	"os"
+	"path/filepath"
 	"strings"
 	"sync"
 	"time"
@@ -30,6 +33,7 @@ import (
 )
 
 const (
+	defaultOCSPStoreDir      = "ocsp"
 	defaultOCSPCheckInterval = 24 * time.Hour
 	minOCSPCheckInterval     = 2 * time.Minute
 )
@@ -92,8 +96,17 @@ func (oc *OCSPMonitor) getNextRun() time.Duration {
 func (oc *OCSPMonitor) getStatus() ([]byte, *ocsp.Response, error) {
 	raw, resp := oc.getCacheStatus()
 	if len(raw) > 0 && resp != nil {
+		// Check if the OCSP is still valid.
+		if err := validOCSPResponse(resp); err == nil {
+			return raw, resp, nil
+		}
+	}
+	var err error
+	raw, resp, err = oc.getLocalStatus()
+	if err == nil {
 		return raw, resp, nil
 	}
+
 	return oc.getRemoteStatus()
 }
 
@@ -103,6 +116,41 @@ func (oc *OCSPMonitor) getCacheStatus() ([]byte, *ocsp.Response) {
 	return oc.raw, oc.resp
 }
 
+func (oc *OCSPMonitor) getLocalStatus() ([]byte, *ocsp.Response, error) {
+	opts := oc.srv.getOpts()
+	storeDir := opts.StoreDir
+	if storeDir == _EMPTY_ {
+		return nil, nil, fmt.Errorf("store_dir not set")
+	}
+
+	// This key must be based upon the current full certificate, not the public key,
+	// so MUST be on the full raw certificate and not an SPKI or other reduced form.
+	key := fmt.Sprintf("%x", sha256.Sum256(oc.Leaf.Raw))
+
+	oc.mu.Lock()
+	raw, err := ioutil.ReadFile(filepath.Join(storeDir, defaultOCSPStoreDir, key))
+	oc.mu.Unlock()
+	if err != nil {
+		return nil, nil, err
+	}
+
+	resp, err := ocsp.ParseResponse(raw, oc.Issuer)
+	if err != nil {
+		return nil, nil, err
+	}
+	if err := validOCSPResponse(resp); err != nil {
+		return nil, nil, err
+	}
+
+	// Cache the response.
+	oc.mu.Lock()
+	oc.raw = raw
+	oc.resp = resp
+	oc.mu.Unlock()
+
+	return raw, resp, nil
+}
+
 func (oc *OCSPMonitor) getRemoteStatus() ([]byte, *ocsp.Response, error) {
 	opts := oc.srv.getOpts()
 	var overrideURLs []string
@@ -163,6 +211,13 @@ func (oc *OCSPMonitor) getRemoteStatus() ([]byte, *ocsp.Response, error) {
 		return nil, nil, err
 	}
 
+	if storeDir := opts.StoreDir; storeDir != _EMPTY_ {
+		key := fmt.Sprintf("%x", sha256.Sum256(oc.Leaf.Raw))
+		if err := oc.writeOCSPStatus(storeDir, key, raw); err != nil {
+			return nil, nil, fmt.Errorf("failed to write ocsp status: %w", err)
+		}
+	}
+
 	oc.mu.Lock()
 	oc.raw = raw
 	oc.resp = resp
@@ -201,7 +256,7 @@ func (oc *OCSPMonitor) run() {
 		return
 	}
 
-	for s.Running() {
+	for {
 		// On reload, if the certificate changes then need to stop this monitor.
 		select {
 		case <-time.After(nextRun):
@@ -294,6 +349,10 @@ func (srv *Server) NewOCSPMonitor(tc *tls.Config) (*tls.Config, *OCSPMonitor, er
 			return tc, nil, nil
 		}
 
+		if err := srv.setupOCSPStapleStoreDir(); err != nil {
+			return nil, nil, err
+		}
+
 		// TODO: Add OCSP 'responder_cert' option in case CA cert not available.
 		issuer, err := getOCSPIssuer(caFile, cert.Certificate)
 		if err != nil {
@@ -384,6 +443,35 @@ func hasOCSPStatusRequest(cert *x509.Certificate) bool {
 	return false
 }
 
+// writeOCSPStatus writes an OCSP status to a temporary file then moves it to a
+// new path, in an attempt to avoid corrupting existing data.
+func (oc *OCSPMonitor) writeOCSPStatus(storeDir, file string, data []byte) error {
+	storeDir = filepath.Join(storeDir, defaultOCSPStoreDir)
+	tmp, err := ioutil.TempFile(storeDir, "tmp-cert-status")
+	if err != nil {
+		return err
+	}
+
+	if _, err := tmp.Write(data); err != nil {
+		tmp.Close()
+		os.Remove(tmp.Name())
+		return err
+	}
+	if err := tmp.Close(); err != nil {
+		return err
+	}
+
+	oc.mu.Lock()
+	err = os.Rename(tmp.Name(), filepath.Join(storeDir, file))
+	oc.mu.Unlock()
+	if err != nil {
+		os.Remove(tmp.Name())
+		return err
+	}
+
+	return nil
+}
+
 func parseCertPEM(name string) (*x509.Certificate, error) {
 	data, err := ioutil.ReadFile(name)
 	if err != nil {
diff --git a/server/opts.go b/server/opts.go
index e79541fc..68d86953 100644
--- a/server/opts.go
+++ b/server/opts.go
@@ -793,6 +793,13 @@ func (o *Options) processConfigFileLine(k string, v interface{}, errors *[]error
 			*errors = append(*errors, err)
 			return
 		}
+	case "store_dir", "storedir":
+		// Check if JetStream configuration is also setting the storage directory.
+		if o.StoreDir != "" {
+			*errors = append(*errors, &configErr{tk, "Duplicate 'store_dir' configuration"})
+			return
+		}
+		o.StoreDir = v.(string)
 	case "jetstream":
 		err := parseJetStream(tk, o, errors, warnings)
 		if err != nil {
@@ -1558,6 +1565,10 @@ func parseJetStream(v interface{}, opts *Options, errors *[]error, warnings *[]e
 			tk, mv = unwrapValue(mv, &lt)
 			switch strings.ToLower(mk) {
 			case "store_dir", "storedir":
+				// StoreDir can be set at the top level as well so have to prevent ambiguous declarations.
+				if opts.StoreDir != "" {
+					return &configErr{tk, "Duplicate 'store_dir' configuration"}
+				}
 				opts.StoreDir = mv.(string)
 			case "max_memory_store", "max_mem_store", "max_mem":
 				opts.JetStreamMaxMemory = mv.(int64)
diff --git a/server/reload.go b/server/reload.go
index 5704e90e..ccfec13b 100644
--- a/server/reload.go
+++ b/server/reload.go
@@ -1285,12 +1285,18 @@ func (s *Server) applyOptions(ctx *reloadContext, opts []option) {
 func (s *Server) reloadOCSP() error {
 	opts := s.getOpts()
 
+	if err := s.setupOCSPStapleStoreDir(); err != nil {
+		return err
+	}
+
 	s.mu.Lock()
 	ocsps := s.ocsps
 	s.mu.Unlock()
 
 	// Stop all OCSP Stapling monitors in case there were any running.
+	var wasEnabled bool
 	for _, oc := range ocsps {
+		wasEnabled = true
 		oc.stop()
 	}
 
@@ -1303,15 +1309,17 @@ func (s *Server) reloadOCSP() error {
 		}
 		// Check if an OCSP stapling monitor is required for this certificate.
 		if mon != nil {
+			s.Noticef("OCSP Stapling enabled for client connections")
 			ocspm = append(ocspm, mon)
 
-			// Override the TLS config with one that follows OCSP.
+			// Override the TLS config with one that has OCSP enabled.
 			s.optsMu.Lock()
 			s.opts.TLSConfig = tc
 			s.optsMu.Unlock()
 			s.startGoRoutine(func() { mon.run() })
+		} else if wasEnabled {
+			s.Warnf("OCSP Stapling disabled for client connections")
 		}
-		s.Noticef("OCSP Stapling enabled for client connections")
 	}
 	// Replace stopped monitors with the new ones.
 	s.mu.Lock()
diff --git a/server/server.go b/server/server.go
index a2ef244f..ff1bebb5 100644
--- a/server/server.go
+++ b/server/server.go
@@ -1470,6 +1470,24 @@ func (s *Server) fetchAccount(name string) (*Account, error) {
 	return acc, nil
 }
 
+func (s *Server) setupOCSPStapleStoreDir() error {
+	opts := s.getOpts()
+	storeDir := opts.StoreDir
+	if storeDir == _EMPTY_ {
+		s.Warnf("OCSP Stapling disk cache is disabled (missing 'store_dir')")
+		return nil
+	}
+	storeDir = filepath.Join(storeDir, defaultOCSPStoreDir)
+	if stat, err := os.Stat(storeDir); os.IsNotExist(err) {
+		if err := os.MkdirAll(storeDir, defaultDirPerms); err != nil {
+			return fmt.Errorf("could not create OCSP storage directory - %v", err)
+		}
+	} else if stat == nil || !stat.IsDir() {
+		return fmt.Errorf("OCSP storage directory is not a directory")
+	}
+	return nil
+}
+
 func (s *Server) enableOCSP() error {
 	opts := s.getOpts()
 
@@ -1481,14 +1499,15 @@ func (s *Server) enableOCSP() error {
 		}
 		// Check if an OCSP stapling monitor is required for this certificate.
 		if mon != nil {
+			s.Noticef("OCSP Stapling enabled for client connections")
+
 			s.ocsps = append(s.ocsps, mon)
 			// Override the TLS config with one that follows OCSP.
 			opts.TLSConfig = tc
 			s.startGoRoutine(func() { mon.run() })
 		}
-		s.Noticef("OCSP Stapling enabled for client connections")
 	}
-	// FIXME: Add support for leafnodes, routes, MQTT, WebSocket
+	// FIXME: Add support for leafnodes, routes, gateways, MQTT, WebSocket
 
 	return nil
 }
diff --git a/test/ocsp_test.go b/test/ocsp_test.go
index d852a042..204fb571 100644
--- a/test/ocsp_test.go
+++ b/test/ocsp_test.go
@@ -14,6 +14,7 @@
 package test
 
 import (
+	"bytes"
 	"context"
 	"crypto/rsa"
 	"crypto/tls"
@@ -23,6 +24,8 @@ import (
 	"fmt"
 	"io/ioutil"
 	"net/http"
+	"os"
+	"path/filepath"
 	"strconv"
 	"strings"
 	"sync"
@@ -50,7 +53,11 @@ func TestOCSPAlwaysMustStapleAndShutdown(t *testing.T) {
 	addr := fmt.Sprintf("http://%s", ocspr.Addr)
 	setOCSPStatus(t, addr, serverCert, ocsp.Good)
 
-	opts := DefaultTestOptions
+	opts := server.Options{}
+	opts.Host = "127.0.0.1"
+	opts.NoLog = true
+	opts.NoSigs = true
+	opts.MaxControlLine = 4096
 	opts.Port = -1
 	opts.TLSCert = serverCert
 	opts.TLSKey = serverKey
@@ -140,7 +147,11 @@ func TestOCSPMustStapleShutdown(t *testing.T) {
 	addr := fmt.Sprintf("http://%s", ocspr.Addr)
 	setOCSPStatus(t, addr, serverCert, ocsp.Good)
 
-	opts := DefaultTestOptions
+	opts := server.Options{}
+	opts.Host = "127.0.0.1"
+	opts.NoLog = true
+	opts.NoSigs = true
+	opts.MaxControlLine = 4096
 	opts.Port = -1
 	opts.TLSCert = serverCert
 	opts.TLSKey = serverKey
@@ -321,7 +332,11 @@ func TestOCSPAutoWithoutMustStapleDoesNotShutdownOnRevoke(t *testing.T) {
 	addr := fmt.Sprintf("http://%s", ocspr.Addr)
 	setOCSPStatus(t, addr, serverCert, ocsp.Good)
 
-	opts := DefaultTestOptions
+	opts := server.Options{}
+	opts.Host = "127.0.0.1"
+	opts.NoLog = true
+	opts.NoSigs = true
+	opts.MaxControlLine = 4096
 	opts.Port = -1
 	opts.TLSCert = serverCert
 	opts.TLSKey = serverKey
@@ -663,9 +678,14 @@ func TestOCSPReloadRotateTLSCertDisableMustStaple(t *testing.T) {
 	addr := fmt.Sprintf("http://%s", ocspr.Addr)
 	setOCSPStatus(t, addr, serverCert, ocsp.Good)
 
-	content := `
+	storeDir := createDir(t, "_ocsp")
+	defer removeDir(t, storeDir)
+
+	originalContent := `
 		port: -1
 
+		store_dir: "%s"
+
 		tls {
 			cert_file: "configs/certs/ocsp/server-status-request-url-cert.pem"
 			key_file: "configs/certs/ocsp/server-status-request-url-key.pem"
@@ -673,14 +693,18 @@ func TestOCSPReloadRotateTLSCertDisableMustStaple(t *testing.T) {
 			timeout: 5
 		}
 	`
+
+	content := fmt.Sprintf(originalContent, storeDir)
 	conf := createConfFile(t, []byte(content))
 	defer removeFile(t, conf)
 	s, opts := RunServerWithConfig(conf)
 	defer s.Shutdown()
 
+	var staple []byte
 	nc, err := nats.Connect(fmt.Sprintf("tls://localhost:%d", opts.Port),
 		nats.Secure(&tls.Config{
 			VerifyConnection: func(s tls.ConnectionState) error {
+				staple = s.OCSPResponse
 				resp, err := getOCSPStatus(s)
 				if err != nil {
 					return err
@@ -710,10 +734,37 @@ func TestOCSPReloadRotateTLSCertDisableMustStaple(t *testing.T) {
 	}
 	nc.Close()
 
+	files := []string{}
+	err = filepath.Walk(storeDir+"/ocsp/", func(path string, info os.FileInfo, err error) error {
+		if info.IsDir() {
+			return nil
+		}
+		files = append(files, path)
+		return nil
+	})
+	if err != nil {
+		t.Fatal(err)
+	}
+	found := false
+	for _, file := range files {
+		data, err := ioutil.ReadFile(file)
+		if err != nil {
+			t.Error(err)
+		}
+		if bytes.Equal(staple, data) {
+			found = true
+		}
+	}
+	if !found {
+		t.Error("Could not find OCSP Staple")
+	}
+
 	// Change the contents with another that has OCSP Stapling disabled.
-	content = `
+	updatedContent := `
 		port: -1
 
+		store_dir: "%s"
+
 		tls {
 			cert_file: "configs/certs/ocsp/server-cert.pem"
 			key_file: "configs/certs/ocsp/server-key.pem"
@@ -721,6 +772,7 @@ func TestOCSPReloadRotateTLSCertDisableMustStaple(t *testing.T) {
 			timeout: 5
 		}
 	`
+	content = fmt.Sprintf(updatedContent, storeDir)
 	if err := ioutil.WriteFile(conf, []byte(content), 0666); err != nil {
 		t.Fatalf("Error writing config: %v", err)
 	}
@@ -729,7 +781,7 @@ func TestOCSPReloadRotateTLSCertDisableMustStaple(t *testing.T) {
 	}
 
 	// The new certificate does not have must staple so they will be missing.
-	time.Sleep(2 * time.Second)
+	time.Sleep(4 * time.Second)
 
 	nc, err = nats.Connect(fmt.Sprintf("tls://localhost:%d", opts.Port),
 		nats.Secure(&tls.Config{
@@ -747,6 +799,67 @@ func TestOCSPReloadRotateTLSCertDisableMustStaple(t *testing.T) {
 		t.Fatal(err)
 	}
 	nc.Close()
+
+	// Re-enable OCSP Stapling
+	content = fmt.Sprintf(originalContent, storeDir)
+	if err := ioutil.WriteFile(conf, []byte(content), 0666); err != nil {
+		t.Fatalf("Error writing config: %v", err)
+	}
+	if err := s.Reload(); err != nil {
+		t.Fatal(err)
+	}
+
+	var newStaple []byte
+	nc, err = nats.Connect(fmt.Sprintf("tls://localhost:%d", opts.Port),
+		nats.Secure(&tls.Config{
+			VerifyConnection: func(s tls.ConnectionState) error {
+				newStaple = s.OCSPResponse
+				resp, err := getOCSPStatus(s)
+				if err != nil {
+					return err
+				}
+				if resp.Status != ocsp.Good {
+					t.Errorf("Expected valid OCSP staple status")
+				}
+				return nil
+			},
+		}),
+		nats.RootCAs(caCert),
+		nats.ErrorHandler(noOpErrHandler),
+	)
+	if err != nil {
+		t.Fatal(err)
+	}
+	nc.Close()
+
+	// Confirm that it got a new staple.
+	files = []string{}
+	err = filepath.Walk(storeDir+"/ocsp/", func(path string, info os.FileInfo, err error) error {
+		if info.IsDir() {
+			return nil
+		}
+		files = append(files, path)
+		return nil
+	})
+	if err != nil {
+		t.Fatal(err)
+	}
+	found = false
+	for _, file := range files {
+		data, err := ioutil.ReadFile(file)
+		if err != nil {
+			t.Error(err)
+		}
+		if bytes.Equal(newStaple, data) {
+			found = true
+		}
+	}
+	if !found {
+		t.Error("Could not find OCSP Staple")
+	}
+	if bytes.Equal(staple, newStaple) {
+		t.Error("Expected new OCSP Staple")
+	}
 }
 
 func TestOCSPReloadRotateTLSCertEnableMustStaple(t *testing.T) {