diff --git a/pkg/api/plugin_resource_test.go b/pkg/api/plugin_resource_test.go
index 3aeb39a8bd6..a2d3c93111f 100644
--- a/pkg/api/plugin_resource_test.go
+++ b/pkg/api/plugin_resource_test.go
@@ -14,6 +14,7 @@ import (
 	"github.com/stretchr/testify/require"
 
 	"github.com/grafana/grafana/pkg/infra/db"
+	"github.com/grafana/grafana/pkg/infra/kvstore"
 	"github.com/grafana/grafana/pkg/infra/localcache"
 	"github.com/grafana/grafana/pkg/infra/tracing"
 	"github.com/grafana/grafana/pkg/plugins/backendplugin/coreplugin"
@@ -35,6 +36,7 @@ import (
 	"github.com/grafana/grafana/pkg/services/oauthtoken/oauthtokentest"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/config"
+	"github.com/grafana/grafana/pkg/services/pluginsintegration/keystore"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/pluginaccesscontrol"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/plugincontext"
 	pluginSettings "github.com/grafana/grafana/pkg/services/pluginsintegration/pluginsettings/service"
@@ -65,7 +67,7 @@ func TestCallResource(t *testing.T) {
 	reg := registry.ProvideService()
 	l := loader.ProvideService(pCfg, fakes.NewFakeLicensingService(), signature.NewUnsignedAuthorizer(pCfg),
 		reg, provider.ProvideService(coreRegistry), finder.NewLocalFinder(), fakes.NewFakeRoleRegistry(),
-		assetpath.ProvideService(pluginscdn.ProvideService(pCfg)), signature.ProvideService(pCfg))
+		assetpath.ProvideService(pluginscdn.ProvideService(pCfg)), signature.ProvideService(pCfg, keystore.ProvideService(kvstore.NewFakeKVStore())))
 	srcs := sources.ProvideService(cfg, pCfg)
 	ps, err := store.ProvideService(reg, srcs, l)
 	require.NoError(t, err)
diff --git a/pkg/plugins/ifaces.go b/pkg/plugins/ifaces.go
index 9a523686310..a4ce3c6f736 100644
--- a/pkg/plugins/ifaces.go
+++ b/pkg/plugins/ifaces.go
@@ -148,3 +148,12 @@ type FeatureToggles interface {
 type SignatureCalculator interface {
 	Calculate(ctx context.Context, src PluginSource, plugin FoundPlugin) (Signature, error)
 }
+
+type KeyStore interface {
+	Get(ctx context.Context, key string) (string, bool, error)
+	Set(ctx context.Context, key string, value string) error
+	Del(ctx context.Context, key string) error
+	ListKeys(ctx context.Context) ([]string, error)
+	GetLastUpdated(ctx context.Context) (*time.Time, error)
+	SetLastUpdated(ctx context.Context) error
+}
diff --git a/pkg/plugins/manager/loader/loader_test.go b/pkg/plugins/manager/loader/loader_test.go
index d0dda4d4c51..0fa139bd86b 100644
--- a/pkg/plugins/manager/loader/loader_test.go
+++ b/pkg/plugins/manager/loader/loader_test.go
@@ -2,10 +2,7 @@ package loader
 
 import (
 	"context"
-	"encoding/json"
 	"fmt"
-	"net/http"
-	"net/http/httptest"
 	"os"
 	"path/filepath"
 	"sort"
@@ -15,6 +12,7 @@ import (
 	"github.com/google/go-cmp/cmp/cmpopts"
 	"github.com/stretchr/testify/require"
 
+	"github.com/grafana/grafana/pkg/infra/kvstore"
 	"github.com/grafana/grafana/pkg/plugins"
 	"github.com/grafana/grafana/pkg/plugins/backendplugin"
 	"github.com/grafana/grafana/pkg/plugins/config"
@@ -24,10 +22,9 @@ import (
 	"github.com/grafana/grafana/pkg/plugins/manager/loader/finder"
 	"github.com/grafana/grafana/pkg/plugins/manager/loader/initializer"
 	"github.com/grafana/grafana/pkg/plugins/manager/signature"
-	"github.com/grafana/grafana/pkg/plugins/manager/signature/manifestverifier"
 	"github.com/grafana/grafana/pkg/plugins/manager/sources"
 	"github.com/grafana/grafana/pkg/plugins/pluginscdn"
-	"github.com/grafana/grafana/pkg/services/featuremgmt"
+	"github.com/grafana/grafana/pkg/services/pluginsintegration/keystore"
 	"github.com/grafana/grafana/pkg/setting"
 )
 
@@ -1110,115 +1107,6 @@ func TestLoader_Load_SkipUninitializedPlugins(t *testing.T) {
 	})
 }
 
-func TestLoader_Load_UseAPIForManifestPublicKey(t *testing.T) {
-	t.Run("Load plugin using API manifest", func(t *testing.T) {
-		pluginDir, err := filepath.Abs("../testdata/test-app")
-		if err != nil {
-			t.Errorf("could not construct absolute path of plugin dir")
-			return
-		}
-		expected := []*plugins.Plugin{
-			{
-				JSONData: plugins.JSONData{
-					ID:   "test-app",
-					Type: "app",
-					Name: "Test App",
-					Info: plugins.Info{
-						Author: plugins.InfoLink{
-							Name: "Test Inc.",
-							URL:  "http://test.com",
-						},
-						Description: "Official Grafana Test App & Dashboard bundle",
-						Version:     "1.0.0",
-						Links: []plugins.InfoLink{
-							{Name: "Project site", URL: "http://project.com"},
-							{Name: "License & Terms", URL: "http://license.com"},
-						},
-						Logos: plugins.Logos{
-							Small: "public/plugins/test-app/img/logo_small.png",
-							Large: "public/plugins/test-app/img/logo_large.png",
-						},
-						Screenshots: []plugins.Screenshots{
-							{Path: "public/plugins/test-app/img/screenshot1.png", Name: "img1"},
-							{Path: "public/plugins/test-app/img/screenshot2.png", Name: "img2"},
-						},
-						Updated: "2015-02-10",
-					},
-					Dependencies: plugins.Dependencies{
-						GrafanaVersion: "3.x.x",
-						Plugins: []plugins.Dependency{
-							{Type: "datasource", ID: "graphite", Name: "Graphite", Version: "1.0.0"},
-							{Type: "panel", ID: "graph", Name: "Graph", Version: "1.0.0"},
-						},
-					},
-					Includes: []*plugins.Includes{
-						{Name: "Nginx Connections", Path: "dashboards/connections.json", Type: "dashboard", Role: "Viewer", Slug: "nginx-connections"},
-						{Name: "Nginx Memory", Path: "dashboards/memory.json", Type: "dashboard", Role: "Viewer", Slug: "nginx-memory"},
-						{Name: "Nginx Panel", Type: "panel", Role: "Viewer", Slug: "nginx-panel"},
-						{Name: "Nginx Datasource", Type: "datasource", Role: "Viewer", Slug: "nginx-datasource"},
-					},
-					Backend: false,
-				},
-				FS:            plugins.NewLocalFS(filesInDir(t, pluginDir), pluginDir),
-				Class:         plugins.External,
-				Signature:     plugins.SignatureValid,
-				SignatureType: plugins.GrafanaSignature,
-				SignatureOrg:  "Grafana Labs",
-				Module:        "plugins/test-app/module",
-				BaseURL:       "public/plugins/test-app",
-			},
-		}
-
-		reg := fakes.NewFakePluginRegistry()
-		procPrvdr := fakes.NewFakeBackendProcessProvider()
-		procMgr := fakes.NewFakeProcessManager()
-		apiCalled := false
-		cfg := &config.Cfg{Features: featuremgmt.WithFeatures([]interface{}{"pluginsAPIManifestKey"}...)}
-		s := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
-			if r.URL.Path == "/api/plugins/ci/keys" {
-				w.WriteHeader(http.StatusOK)
-				// Use the hardcoded key
-				k, err := manifestverifier.New(&config.Cfg{}, log.New("test")).GetPublicKey("7e4d0c6a708866e7")
-				require.NoError(t, err)
-				data := struct {
-					Items []manifestverifier.ManifestKeys `json:"items"`
-				}{
-					Items: []manifestverifier.ManifestKeys{{PublicKey: k, KeyID: "7e4d0c6a708866e7"}},
-				}
-				b, err := json.Marshal(data)
-				require.NoError(t, err)
-				_, err = w.Write(b)
-				require.NoError(t, err)
-				apiCalled = true
-				return
-			}
-			w.WriteHeader(http.StatusNotFound)
-		}))
-		cfg.GrafanaComURL = s.URL
-		l := newLoader(cfg, func(l *Loader) {
-			l.pluginRegistry = reg
-			l.processManager = procMgr
-			l.pluginInitializer = initializer.New(cfg, procPrvdr, fakes.NewFakeLicensingService())
-		})
-		got, err := l.Load(context.Background(), &fakes.FakePluginSource{
-			PluginClassFunc: func(ctx context.Context) plugins.Class {
-				return plugins.External
-			},
-			PluginURIsFunc: func(ctx context.Context) []string {
-				return []string{pluginDir}
-			},
-		})
-		require.NoError(t, err)
-		require.True(t, apiCalled)
-
-		if !cmp.Equal(got, expected, compareOpts...) {
-			t.Fatalf("Result mismatch (-want +got):\n%s", cmp.Diff(got, expected, compareOpts...))
-		}
-
-		verifyState(t, expected, reg, procPrvdr, procMgr)
-	})
-}
-
 func TestLoader_Load_NestedPlugins(t *testing.T) {
 	rootDir, err := filepath.Abs("../")
 	if err != nil {
@@ -1533,7 +1421,8 @@ func Test_setPathsBasedOnApp(t *testing.T) {
 func newLoader(cfg *config.Cfg, cbs ...func(loader *Loader)) *Loader {
 	l := New(cfg, &fakes.FakeLicensingService{}, signature.NewUnsignedAuthorizer(cfg), fakes.NewFakePluginRegistry(),
 		fakes.NewFakeBackendProcessProvider(), fakes.NewFakeProcessManager(), fakes.NewFakeRoleRegistry(),
-		assetpath.ProvideService(pluginscdn.ProvideService(cfg)), finder.NewLocalFinder(), signature.ProvideService(cfg))
+		assetpath.ProvideService(pluginscdn.ProvideService(cfg)), finder.NewLocalFinder(),
+		signature.ProvideService(cfg, keystore.ProvideService(kvstore.NewFakeKVStore())))
 
 	for _, cb := range cbs {
 		cb(l)
diff --git a/pkg/plugins/manager/manager_integration_test.go b/pkg/plugins/manager/manager_integration_test.go
index d98e34ccfb6..1e20c169614 100644
--- a/pkg/plugins/manager/manager_integration_test.go
+++ b/pkg/plugins/manager/manager_integration_test.go
@@ -14,6 +14,7 @@ import (
 	"gopkg.in/ini.v1"
 
 	"github.com/grafana/grafana/pkg/infra/db"
+	"github.com/grafana/grafana/pkg/infra/kvstore"
 	"github.com/grafana/grafana/pkg/infra/tracing"
 	"github.com/grafana/grafana/pkg/plugins"
 	"github.com/grafana/grafana/pkg/plugins/backendplugin/coreplugin"
@@ -31,6 +32,7 @@ import (
 	"github.com/grafana/grafana/pkg/services/featuremgmt"
 	"github.com/grafana/grafana/pkg/services/licensing"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/config"
+	"github.com/grafana/grafana/pkg/services/pluginsintegration/keystore"
 	plicensing "github.com/grafana/grafana/pkg/services/pluginsintegration/licensing"
 	"github.com/grafana/grafana/pkg/services/searchV2"
 	"github.com/grafana/grafana/pkg/setting"
@@ -117,7 +119,7 @@ func TestIntegrationPluginManager(t *testing.T) {
 	lic := plicensing.ProvideLicensing(cfg, &licensing.OSSLicensingService{Cfg: cfg})
 	l := loader.ProvideService(pCfg, lic, signature.NewUnsignedAuthorizer(pCfg),
 		reg, provider.ProvideService(coreRegistry), finder.NewLocalFinder(), fakes.NewFakeRoleRegistry(),
-		assetpath.ProvideService(pluginscdn.ProvideService(pCfg)), signature.ProvideService(pCfg))
+		assetpath.ProvideService(pluginscdn.ProvideService(pCfg)), signature.ProvideService(pCfg, keystore.ProvideService(kvstore.NewFakeKVStore())))
 	srcs := sources.ProvideService(cfg, pCfg)
 	ps, err := store.ProvideService(reg, srcs, l)
 	require.NoError(t, err)
diff --git a/pkg/plugins/manager/signature/manifest.go b/pkg/plugins/manager/signature/manifest.go
index 7fe263ed9ed..2f4bbcf853f 100644
--- a/pkg/plugins/manager/signature/manifest.go
+++ b/pkg/plugins/manager/signature/manifest.go
@@ -58,17 +58,25 @@ type Signature struct {
 
 var _ plugins.SignatureCalculator = &Signature{}
 
-func ProvideService(cfg *config.Cfg) *Signature {
+func ProvideService(cfg *config.Cfg, kv plugins.KeyStore) *Signature {
 	log := log.New("plugin.signature")
 	return &Signature{
-		verifier: manifestverifier.New(cfg, log),
+		verifier: manifestverifier.New(cfg, log, kv),
 		mlog:     log,
 	}
 }
 
+func (s *Signature) IsDisabled() bool {
+	return s.verifier.IsDisabled()
+}
+
+func (s *Signature) Run(ctx context.Context) error {
+	return s.verifier.Run(ctx)
+}
+
 // readPluginManifest attempts to read and verify the plugin manifest
 // if any error occurs or the manifest is not valid, this will return an error
-func (s *Signature) readPluginManifest(body []byte) (*PluginManifest, error) {
+func (s *Signature) readPluginManifest(ctx context.Context, body []byte) (*PluginManifest, error) {
 	block, _ := clearsign.Decode(body)
 	if block == nil {
 		return nil, errors.New("unable to decode manifest")
@@ -81,7 +89,7 @@ func (s *Signature) readPluginManifest(body []byte) (*PluginManifest, error) {
 		return nil, fmt.Errorf("%v: %w", "Error parsing manifest JSON", err)
 	}
 
-	if err = s.validateManifest(manifest, block); err != nil {
+	if err = s.validateManifest(ctx, manifest, block); err != nil {
 		return nil, err
 	}
 
@@ -131,7 +139,7 @@ func (s *Signature) Calculate(ctx context.Context, src plugins.PluginSource, plu
 		}, nil
 	}
 
-	manifest, err := s.readPluginManifest(byteValue)
+	manifest, err := s.readPluginManifest(ctx, byteValue)
 	if err != nil {
 		s.mlog.Debug("Plugin signature invalid", "id", plugin.JSONData.ID, "err", err)
 		return plugins.Signature{
@@ -286,7 +294,7 @@ func (r invalidFieldErr) Error() string {
 	return fmt.Sprintf("valid manifest field %s is required", r.field)
 }
 
-func (s *Signature) validateManifest(m PluginManifest, block *clearsign.Block) error {
+func (s *Signature) validateManifest(ctx context.Context, m PluginManifest, block *clearsign.Block) error {
 	if len(m.Plugin) == 0 {
 		return invalidFieldErr{field: "plugin"}
 	}
@@ -314,5 +322,5 @@ func (s *Signature) validateManifest(m PluginManifest, block *clearsign.Block) e
 		}
 	}
 
-	return s.verifier.Verify(m.KeyID, block)
+	return s.verifier.Verify(ctx, m.KeyID, block)
 }
diff --git a/pkg/plugins/manager/signature/manifest_test.go b/pkg/plugins/manager/signature/manifest_test.go
index 3a1e887ffa8..5c9d78f7d37 100644
--- a/pkg/plugins/manager/signature/manifest_test.go
+++ b/pkg/plugins/manager/signature/manifest_test.go
@@ -10,9 +10,11 @@ import (
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
 
+	"github.com/grafana/grafana/pkg/infra/kvstore"
 	"github.com/grafana/grafana/pkg/plugins"
 	"github.com/grafana/grafana/pkg/plugins/config"
 	"github.com/grafana/grafana/pkg/plugins/manager/fakes"
+	"github.com/grafana/grafana/pkg/services/pluginsintegration/keystore"
 	"github.com/grafana/grafana/pkg/setting"
 )
 
@@ -49,8 +51,8 @@ NR7DnB0CCQHO+4FlSPtXFTzNepoc+CytQyDAeOLMLmf2Tqhk2YShk+G/YlVX
 -----END PGP SIGNATURE-----`
 
 	t.Run("valid manifest", func(t *testing.T) {
-		s := ProvideService(&config.Cfg{})
-		manifest, err := s.readPluginManifest([]byte(txt))
+		s := ProvideService(&config.Cfg{}, keystore.ProvideService(kvstore.NewFakeKVStore()))
+		manifest, err := s.readPluginManifest(context.Background(), []byte(txt))
 
 		require.NoError(t, err)
 		require.NotNil(t, manifest)
@@ -66,8 +68,8 @@ NR7DnB0CCQHO+4FlSPtXFTzNepoc+CytQyDAeOLMLmf2Tqhk2YShk+G/YlVX
 
 	t.Run("invalid manifest", func(t *testing.T) {
 		modified := strings.ReplaceAll(txt, "README.md", "xxxxxxxxxx")
-		s := ProvideService(&config.Cfg{})
-		_, err := s.readPluginManifest([]byte(modified))
+		s := ProvideService(&config.Cfg{}, keystore.ProvideService(kvstore.NewFakeKVStore()))
+		_, err := s.readPluginManifest(context.Background(), []byte(modified))
 		require.Error(t, err)
 	})
 }
@@ -104,8 +106,8 @@ khdr/tZ1PDgRxMqB/u+Vtbpl0xSxgblnrDOYMSI=
 -----END PGP SIGNATURE-----`
 
 	t.Run("valid manifest", func(t *testing.T) {
-		s := ProvideService(&config.Cfg{})
-		manifest, err := s.readPluginManifest([]byte(txt))
+		s := ProvideService(&config.Cfg{}, keystore.ProvideService(kvstore.NewFakeKVStore()))
+		manifest, err := s.readPluginManifest(context.Background(), []byte(txt))
 
 		require.NoError(t, err)
 		require.NotNil(t, manifest)
@@ -158,7 +160,7 @@ func TestCalculate(t *testing.T) {
 			setting.AppUrl = tc.appURL
 
 			basePath := filepath.Join(parentDir, "testdata/non-pvt-with-root-url/plugin")
-			s := ProvideService(&config.Cfg{})
+			s := ProvideService(&config.Cfg{}, keystore.ProvideService(kvstore.NewFakeKVStore()))
 			sig, err := s.Calculate(context.Background(), &fakes.FakePluginSource{
 				PluginClassFunc: func(ctx context.Context) plugins.Class {
 					return plugins.External
@@ -189,7 +191,7 @@ func TestCalculate(t *testing.T) {
 		basePath := "../testdata/renderer-added-file/plugin"
 
 		runningWindows = true
-		s := ProvideService(&config.Cfg{})
+		s := ProvideService(&config.Cfg{}, keystore.ProvideService(kvstore.NewFakeKVStore()))
 		sig, err := s.Calculate(context.Background(), &fakes.FakePluginSource{
 			PluginClassFunc: func(ctx context.Context) plugins.Class {
 				return plugins.External
@@ -238,7 +240,7 @@ func TestCalculate(t *testing.T) {
 
 				basePath := "../testdata/app-with-child/dist"
 
-				s := ProvideService(&config.Cfg{})
+				s := ProvideService(&config.Cfg{}, keystore.ProvideService(kvstore.NewFakeKVStore()))
 				sig, err := s.Calculate(context.Background(), &fakes.FakePluginSource{
 					PluginClassFunc: func(ctx context.Context) plugins.Class {
 						return plugins.External
@@ -683,8 +685,8 @@ func Test_validateManifest(t *testing.T) {
 	}
 	for _, tc := range tcs {
 		t.Run(tc.name, func(t *testing.T) {
-			s := ProvideService(&config.Cfg{})
-			err := s.validateManifest(*tc.manifest, nil)
+			s := ProvideService(&config.Cfg{}, keystore.ProvideService(kvstore.NewFakeKVStore()))
+			err := s.validateManifest(context.Background(), *tc.manifest, nil)
 			require.Errorf(t, err, tc.expectedErr)
 		})
 	}
diff --git a/pkg/plugins/manager/signature/manifestverifier/verifier.go b/pkg/plugins/manager/signature/manifestverifier/verifier.go
index a5cd6ce57cb..4424b8a8e42 100644
--- a/pkg/plugins/manager/signature/manifestverifier/verifier.go
+++ b/pkg/plugins/manager/signature/manifestverifier/verifier.go
@@ -2,6 +2,7 @@ package manifestverifier
 
 import (
 	"bytes"
+	"context"
 	"encoding/json"
 	"errors"
 	"fmt"
@@ -14,10 +15,16 @@ import (
 	"github.com/ProtonMail/go-crypto/openpgp"
 	"github.com/ProtonMail/go-crypto/openpgp/clearsign"
 	"github.com/ProtonMail/go-crypto/openpgp/packet"
+	"github.com/grafana/grafana/pkg/plugins"
 	"github.com/grafana/grafana/pkg/plugins/config"
 	"github.com/grafana/grafana/pkg/plugins/log"
+
+	// Only used for getting the feature flag value
+	"github.com/grafana/grafana/pkg/services/featuremgmt"
 )
 
+const publicKeySyncInterval = 10 * 24 * time.Hour // 10 days
+
 // ManifestKeys is the database representation of public keys
 // used to verify plugin manifests.
 type ManifestKeys struct {
@@ -30,20 +37,82 @@ type ManifestVerifier struct {
 	cfg  *config.Cfg
 	mlog log.Logger
 
-	lock       sync.Mutex
-	cli        http.Client
-	publicKeys map[string]ManifestKeys
+	lock    sync.Mutex
+	cli     http.Client
+	kv      plugins.KeyStore
+	hasKeys bool
 }
 
-func New(cfg *config.Cfg, mlog log.Logger) *ManifestVerifier {
-	return &ManifestVerifier{
-		cfg:        cfg,
-		publicKeys: map[string]ManifestKeys{},
-		mlog:       mlog,
-		cli:        makeHttpClient(),
+func New(cfg *config.Cfg, mlog log.Logger, kv plugins.KeyStore) *ManifestVerifier {
+	pmv := &ManifestVerifier{
+		cfg:  cfg,
+		mlog: mlog,
+		cli:  makeHttpClient(),
+		kv:   kv,
 	}
+	return pmv
 }
 
+// IsDisabled disables dynamic retrieval of public keys from the API server.
+func (pmv *ManifestVerifier) IsDisabled() bool {
+	return pmv.cfg == nil || pmv.cfg.Features == nil || !pmv.cfg.Features.IsEnabled(featuremgmt.FlagPluginsAPIManifestKey)
+}
+
+func (pmv *ManifestVerifier) Run(ctx context.Context) error {
+	// do an initial update if necessary
+	err := pmv.updateKeys(ctx)
+	if err != nil {
+		pmv.mlog.Error("Error downloading plugin manifest keys", "error", err)
+	}
+
+	// calculate initial send delay
+	lastUpdated, err := pmv.kv.GetLastUpdated(ctx)
+	if err != nil {
+		return err
+	}
+	nextSendInterval := time.Until(lastUpdated.Add(publicKeySyncInterval))
+	if nextSendInterval < time.Minute {
+		nextSendInterval = time.Minute
+	}
+
+	downloadKeysTicker := time.NewTicker(nextSendInterval)
+	defer downloadKeysTicker.Stop()
+
+	select {
+	case <-downloadKeysTicker.C:
+		err = pmv.updateKeys(ctx)
+		if err != nil {
+			pmv.mlog.Error("Error downloading plugin manifest keys", "error", err)
+		}
+
+		if nextSendInterval != publicKeySyncInterval {
+			nextSendInterval = publicKeySyncInterval
+			downloadKeysTicker.Reset(nextSendInterval)
+		}
+	case <-ctx.Done():
+		return ctx.Err()
+	}
+
+	return ctx.Err()
+}
+
+func (pmv *ManifestVerifier) updateKeys(ctx context.Context) error {
+	pmv.lock.Lock()
+	defer pmv.lock.Unlock()
+
+	lastUpdated, err := pmv.kv.GetLastUpdated(ctx)
+	if err != nil {
+		return err
+	}
+	if time.Since(*lastUpdated) < publicKeySyncInterval {
+		// Cache is still valid
+		return nil
+	}
+
+	return pmv.downloadKeys(ctx)
+}
+
+const publicKeyID = "7e4d0c6a708866e7"
 const publicKeyText = `-----BEGIN PGP PUBLIC KEY BLOCK-----
 Version: OpenPGP.js v4.10.1
 Comment: https://openpgpjs.org
@@ -68,40 +137,24 @@ N1c5v9v/4h6qeA==
 -----END PGP PUBLIC KEY BLOCK-----
 `
 
-// getPublicKey loads public keys from:
-//   - The hard-coded value if the feature flag is not enabled.
-//   - A cached value from memory if it has been already retrieved.
-//   - The Grafana.com API if the database is empty.
-func (pmv *ManifestVerifier) GetPublicKey(keyID string) (string, error) {
-	if pmv.cfg == nil || pmv.cfg.Features == nil || !pmv.cfg.Features.IsEnabled("pluginsAPIManifestKey") {
-		return publicKeyText, nil
-	}
-
-	pmv.lock.Lock()
-	defer pmv.lock.Unlock()
-
-	key, exist := pmv.publicKeys[keyID]
-	if exist {
-		return key.PublicKey, nil
-	}
-
-	// Retrieve the key from the API and store it in the database
+// Retrieve the key from the API and store it in the database
+func (pmv *ManifestVerifier) downloadKeys(ctx context.Context) error {
 	var data struct {
 		Items []ManifestKeys
 	}
 
 	url, err := url.JoinPath(pmv.cfg.GrafanaComURL, "/api/plugins/ci/keys") // nolint:gosec URL is provided by config
 	if err != nil {
-		return "", err
+		return err
 	}
-	req, err := http.NewRequest(http.MethodGet, url, nil)
+	req, err := http.NewRequestWithContext(ctx, http.MethodGet, url, nil)
 	if err != nil {
-		return "", err
+		return err
 	}
 
 	resp, err := pmv.cli.Do(req)
 	if err != nil {
-		return "", err
+		return err
 	}
 	defer func() {
 		err := resp.Body.Close()
@@ -111,27 +164,89 @@ func (pmv *ManifestVerifier) GetPublicKey(keyID string) (string, error) {
 	}()
 
 	if err := json.NewDecoder(resp.Body).Decode(&data); err != nil {
-		return "", err
+		return err
 	}
 
 	if len(data.Items) == 0 {
-		return "", errors.New("missing public key")
+		return errors.New("missing public key")
 	}
 
+	cachedKeys, err := pmv.kv.ListKeys(ctx)
+	if err != nil {
+		return err
+	}
+
+	shouldKeep := make(map[string]bool)
 	for _, key := range data.Items {
-		pmv.publicKeys[key.KeyID] = key
+		err = pmv.kv.Set(ctx, key.KeyID, key.PublicKey)
+		if err != nil {
+			return err
+		}
+		shouldKeep[key.KeyID] = true
 	}
 
-	key, exist = pmv.publicKeys[keyID]
+	// Delete keys that are no longer in the API
+	for _, key := range cachedKeys {
+		if !shouldKeep[key] {
+			err = pmv.kv.Del(ctx, key)
+			if err != nil {
+				return err
+			}
+		}
+	}
+
+	// Update the last updated timestamp
+	return pmv.kv.SetLastUpdated(ctx)
+}
+
+func (pmv *ManifestVerifier) ensureKeys(ctx context.Context) error {
+	if pmv.hasKeys {
+		return nil
+	}
+	keys, err := pmv.kv.ListKeys(ctx)
+	if err != nil {
+		return err
+	}
+	if len(keys) == 0 {
+		// Populate with the default key
+		err := pmv.kv.Set(ctx, publicKeyID, publicKeyText)
+		if err != nil {
+			return err
+		}
+	}
+	pmv.hasKeys = true
+	return nil
+}
+
+// getPublicKey loads public keys from:
+//   - The hard-coded value if the feature flag is not enabled.
+//   - A cached value from kv storage if it has been already retrieved. This cache is populated from the grafana.com API.
+func (pmv *ManifestVerifier) getPublicKey(ctx context.Context, keyID string) (string, error) {
+	if pmv.IsDisabled() {
+		return publicKeyText, nil
+	}
+
+	pmv.lock.Lock()
+	defer pmv.lock.Unlock()
+
+	err := pmv.ensureKeys(ctx)
+	if err != nil {
+		return "", err
+	}
+
+	key, exist, err := pmv.kv.Get(ctx, keyID)
+	if err != nil {
+		return "", err
+	}
 	if exist {
-		return key.PublicKey, nil
+		return key, nil
 	}
 
 	return "", fmt.Errorf("missing public key for %s", keyID)
 }
 
-func (pmv *ManifestVerifier) Verify(keyID string, block *clearsign.Block) error {
-	publicKey, err := pmv.GetPublicKey(keyID)
+func (pmv *ManifestVerifier) Verify(ctx context.Context, keyID string, block *clearsign.Block) error {
+	publicKey, err := pmv.getPublicKey(ctx, keyID)
 	if err != nil {
 		return err
 	}
diff --git a/pkg/plugins/manager/signature/manifestverifier/verifier_test.go b/pkg/plugins/manager/signature/manifestverifier/verifier_test.go
index 116d447b3d2..2d5ed092d22 100644
--- a/pkg/plugins/manager/signature/manifestverifier/verifier_test.go
+++ b/pkg/plugins/manager/signature/manifestverifier/verifier_test.go
@@ -1,22 +1,26 @@
 package manifestverifier
 
 import (
+	"context"
 	"encoding/json"
 	"net/http"
 	"net/http/httptest"
 	"os"
 	"testing"
+	"time"
 
 	"github.com/ProtonMail/go-crypto/openpgp/clearsign"
+	"github.com/grafana/grafana/pkg/infra/kvstore"
 	"github.com/grafana/grafana/pkg/plugins/config"
 	"github.com/grafana/grafana/pkg/plugins/log"
 	"github.com/grafana/grafana/pkg/services/featuremgmt"
+	"github.com/grafana/grafana/pkg/services/pluginsintegration/keystore"
 	"github.com/stretchr/testify/require"
 )
 
 func Test_Verify(t *testing.T) {
 	t.Run("it should verify a manifest with the default key", func(t *testing.T) {
-		v := New(&config.Cfg{}, log.New("test"))
+		v := New(&config.Cfg{}, log.New("test"), keystore.ProvideService(kvstore.NewFakeKVStore()))
 
 		body, err := os.ReadFile("../../testdata/test-app/MANIFEST.txt")
 		if err != nil {
@@ -28,47 +32,107 @@ func Test_Verify(t *testing.T) {
 			t.Fatal("failed to decode")
 		}
 
-		err = v.Verify("7e4d0c6a708866e7", block)
+		err = v.Verify(context.Background(), "7e4d0c6a708866e7", block)
 		require.NoError(t, err)
 	})
-
-	t.Run("it should verify a manifest with the API key", func(t *testing.T) {
-		cfg := &config.Cfg{
-			Features: featuremgmt.WithFeatures([]interface{}{"pluginsAPIManifestKey"}...),
-		}
-		v := New(cfg, log.New("test"))
-		apiCalled := false
-		s := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
-			if r.URL.Path == "/api/plugins/ci/keys" {
-				w.WriteHeader(http.StatusOK)
-				data := struct {
-					Items []ManifestKeys `json:"items"`
-				}{
-					Items: []ManifestKeys{{PublicKey: publicKeyText, KeyID: "7e4d0c6a708866e7"}},
-				}
-				b, err := json.Marshal(data)
-				require.NoError(t, err)
-				_, err = w.Write(b)
-				require.NoError(t, err)
-				apiCalled = true
-				return
-			}
-			w.WriteHeader(http.StatusNotFound)
-		}))
-		cfg.GrafanaComURL = s.URL
-
-		body, err := os.ReadFile("../../testdata/test-app/MANIFEST.txt")
-		if err != nil {
-			t.Fatal(err)
-		}
-
-		block, _ := clearsign.Decode(body)
-		if block == nil {
-			t.Fatal("failed to decode")
-		}
-
-		err = v.Verify("7e4d0c6a708866e7", block)
-		require.NoError(t, err)
-		require.Equal(t, true, apiCalled)
-	})
+}
+
+func setFakeAPIServer(t *testing.T, publicKey string, keyID string) (*httptest.Server, chan bool) {
+	done := make(chan bool)
+	return httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		if r.URL.Path == "/api/plugins/ci/keys" {
+			w.WriteHeader(http.StatusOK)
+			data := struct {
+				Items []ManifestKeys `json:"items"`
+			}{
+				Items: []ManifestKeys{{PublicKey: publicKey, KeyID: keyID}},
+			}
+			b, err := json.Marshal(data)
+			if err != nil {
+				t.Fatal(err)
+			}
+			_, err = w.Write(b)
+			if err != nil {
+				t.Fatal(err)
+			}
+			require.NoError(t, err)
+			done <- true
+			return
+		}
+		w.WriteHeader(http.StatusNotFound)
+		done <- true
+	})), done
+}
+func Test_PublicKeyUpdate(t *testing.T) {
+	t.Run("it should verify a manifest with the API key", func(t *testing.T) {
+		cfg := &config.Cfg{
+			Features: featuremgmt.WithFeatures([]interface{}{featuremgmt.FlagPluginsAPIManifestKey}...),
+		}
+		expectedKey := "fake"
+		s, done := setFakeAPIServer(t, expectedKey, "7e4d0c6a708866e7")
+		cfg.GrafanaComURL = s.URL
+		v := New(cfg, log.New("test"), keystore.ProvideService(kvstore.NewFakeKVStore()))
+		go func() {
+			err := v.Run(context.Background())
+			require.NoError(t, err)
+		}()
+		<-done
+
+		// wait for the lock to be free
+		v.lock.Lock()
+		defer v.lock.Unlock()
+		res, found, err := v.kv.Get(context.Background(), "7e4d0c6a708866e7")
+		require.NoError(t, err)
+		require.Equal(t, true, found)
+		require.Equal(t, expectedKey, res)
+	})
+
+	t.Run("it should update the latest update date", func(t *testing.T) {
+		cfg := &config.Cfg{
+			Features: featuremgmt.WithFeatures([]interface{}{featuremgmt.FlagPluginsAPIManifestKey}...),
+		}
+		expectedKey := "fake"
+		s, done := setFakeAPIServer(t, expectedKey, "7e4d0c6a708866e7")
+		cfg.GrafanaComURL = s.URL
+		v := New(cfg, log.New("test"), keystore.ProvideService(kvstore.NewFakeKVStore()))
+		go func() {
+			err := v.Run(context.Background())
+			require.NoError(t, err)
+		}()
+		<-done
+
+		// wait for the lock to be free
+		v.lock.Lock()
+		defer v.lock.Unlock()
+		ti, err := v.kv.GetLastUpdated(context.Background())
+		require.NoError(t, err)
+		require.Less(t, time.Time{}, *ti)
+	})
+
+	t.Run("it should remove old keys", func(t *testing.T) {
+		cfg := &config.Cfg{
+			Features: featuremgmt.WithFeatures([]interface{}{featuremgmt.FlagPluginsAPIManifestKey}...),
+		}
+		expectedKey := "fake"
+		s, done := setFakeAPIServer(t, expectedKey, "other")
+		cfg.GrafanaComURL = s.URL
+		v := New(cfg, log.New("test"), keystore.ProvideService(kvstore.NewFakeKVStore()))
+		go func() {
+			err := v.Run(context.Background())
+			require.NoError(t, err)
+		}()
+		<-done
+
+		// wait for the lock to be free
+		v.lock.Lock()
+		defer v.lock.Unlock()
+		_, found, err := v.kv.Get(context.Background(), "7e4d0c6a708866e7")
+		require.NoError(t, err)
+		require.Equal(t, false, found)
+
+		res, found, err := v.kv.Get(context.Background(), "other")
+		require.NoError(t, err)
+		require.Equal(t, true, found)
+		require.Equal(t, expectedKey, res)
+	})
 }
diff --git a/pkg/server/backgroundsvcs/background_services.go b/pkg/server/backgroundsvcs/background_services.go
index 70e25fb1465..1900d9e455f 100644
--- a/pkg/server/backgroundsvcs/background_services.go
+++ b/pkg/server/backgroundsvcs/background_services.go
@@ -8,6 +8,7 @@ import (
 	uss "github.com/grafana/grafana/pkg/infra/usagestats/service"
 	"github.com/grafana/grafana/pkg/infra/usagestats/statscollector"
 	"github.com/grafana/grafana/pkg/plugins/manager/process"
+	"github.com/grafana/grafana/pkg/plugins/manager/signature"
 	"github.com/grafana/grafana/pkg/registry"
 	"github.com/grafana/grafana/pkg/services/alerting"
 	"github.com/grafana/grafana/pkg/services/auth"
@@ -50,6 +51,7 @@ func ProvideBackgroundServiceRegistry(
 	grpcServerProvider grpcserver.Provider, secretMigrationProvider secretsMigrations.SecretMigrationProvider, loginAttemptService *loginattemptimpl.Service,
 	bundleService *supportbundlesimpl.Service,
 	publicDashboardsMetric *publicdashboardsmetric.Service,
+	signature *signature.Signature,
 	// Need to make sure these are initialized, is there a better place to put them?
 	_ dashboardsnapshots.Service, _ *alerting.AlertNotificationService,
 	_ serviceaccounts.Service, _ *guardian.Provider,
@@ -86,6 +88,7 @@ func ProvideBackgroundServiceRegistry(
 		loginAttemptService,
 		bundleService,
 		publicDashboardsMetric,
+		signature,
 	)
 }
 
diff --git a/pkg/services/pluginsintegration/keystore/keystore.go b/pkg/services/pluginsintegration/keystore/keystore.go
new file mode 100644
index 00000000000..80b5bf5c4ff
--- /dev/null
+++ b/pkg/services/pluginsintegration/keystore/keystore.go
@@ -0,0 +1,74 @@
+package keystore
+
+import (
+	"context"
+	"fmt"
+	"time"
+
+	"github.com/grafana/grafana/pkg/infra/kvstore"
+	"github.com/grafana/grafana/pkg/plugins"
+)
+
+// Service is a service for storing and retrieving public keys.
+type Service struct {
+	kv *kvstore.NamespacedKVStore
+}
+
+const (
+	prefix         = "key-"
+	lastUpdatedKey = "last_updated"
+)
+
+var _ plugins.KeyStore = (*Service)(nil)
+
+func ProvideService(kv kvstore.KVStore) *Service {
+	return &Service{
+		kv: kvstore.WithNamespace(kv, 0, "plugin.publickeys"),
+	}
+}
+
+func (s *Service) Get(ctx context.Context, key string) (string, bool, error) {
+	return s.kv.Get(ctx, prefix+key)
+}
+
+func (s *Service) Set(ctx context.Context, key string, value string) error {
+	return s.kv.Set(ctx, prefix+key, value)
+}
+
+func (s *Service) Del(ctx context.Context, key string) error {
+	return s.kv.Del(ctx, prefix+key)
+}
+
+func (s *Service) GetLastUpdated(ctx context.Context) (*time.Time, error) {
+	lastUpdated := &time.Time{}
+	if val, ok, err := s.kv.Get(ctx, lastUpdatedKey); err != nil {
+		return nil, fmt.Errorf("failed to get last updated time: %v", err)
+	} else if ok {
+		if parsed, err := time.Parse(time.RFC3339, val); err != nil {
+			return nil, fmt.Errorf("failed to parse last updated time: %v", err)
+		} else {
+			lastUpdated = &parsed
+		}
+	}
+	return lastUpdated, nil
+}
+
+func (s *Service) SetLastUpdated(ctx context.Context) error {
+	lastUpdated := time.Now()
+	if err := s.kv.Set(ctx, lastUpdatedKey, lastUpdated.Format(time.RFC3339)); err != nil {
+		return fmt.Errorf("failed to update last updated time: %v", err)
+	}
+	return nil
+}
+
+func (s *Service) ListKeys(ctx context.Context) ([]string, error) {
+	keys, err := s.kv.Keys(ctx, prefix)
+	if err != nil {
+		return nil, err
+	}
+	res := make([]string, 0, len(keys))
+	for _, key := range keys {
+		res = append(res, key.Key)
+	}
+	return res, nil
+}
diff --git a/pkg/services/pluginsintegration/pluginsintegration.go b/pkg/services/pluginsintegration/pluginsintegration.go
index bc4ab99eb47..12770e78a81 100644
--- a/pkg/services/pluginsintegration/pluginsintegration.go
+++ b/pkg/services/pluginsintegration/pluginsintegration.go
@@ -26,6 +26,7 @@ import (
 	"github.com/grafana/grafana/pkg/services/oauthtoken"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/clientmiddleware"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/config"
+	"github.com/grafana/grafana/pkg/services/pluginsintegration/keystore"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/licensing"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/plugincontext"
 	"github.com/grafana/grafana/pkg/services/pluginsintegration/pluginsettings"
@@ -68,6 +69,8 @@ var WireSet = wire.NewSet(
 	wire.Bind(new(plugins.FileStore), new(*filestore.Service)),
 	wire.Bind(new(plugins.SignatureCalculator), new(*signature.Signature)),
 	signature.ProvideService,
+	wire.Bind(new(plugins.KeyStore), new(*keystore.Service)),
+	keystore.ProvideService,
 )
 
 // WireExtensionSet provides a wire.ProviderSet of plugin providers that can be