diff --git a/agent/proxycfg-sources/local/sync.go b/agent/proxycfg-sources/local/sync.go
index c6cee8c61d159..ccaf6403918ca 100644
--- a/agent/proxycfg-sources/local/sync.go
+++ b/agent/proxycfg-sources/local/sync.go
@@ -2,6 +2,7 @@ package local
 
 import (
 	"context"
+	"time"
 
 	"github.com/hashicorp/go-hclog"
 
@@ -50,12 +51,15 @@ func Sync(ctx context.Context, cfg SyncConfig) {
 	cfg.State.Notify(stateCh)
 	defer cfg.State.StopNotify(stateCh)
 
+	const resyncFrequency = 30 * time.Second
+
 	for {
 		sync(cfg)
 
 		select {
 		case <-stateCh:
 			// Wait for a state change.
+		case <-time.After(resyncFrequency):
 		case <-ctx.Done():
 			return
 		}
diff --git a/agent/proxycfg/manager.go b/agent/proxycfg/manager.go
index c58268e7e039b..d21ff4f1ea5bd 100644
--- a/agent/proxycfg/manager.go
+++ b/agent/proxycfg/manager.go
@@ -158,7 +158,7 @@ func (m *Manager) Register(id ProxyID, ns *structs.NodeService, source ProxySour
 
 func (m *Manager) register(id ProxyID, ns *structs.NodeService, source ProxySource, token string, overwrite bool) error {
 	state, ok := m.proxies[id]
-	if ok {
+	if ok && !state.stoppedRunning() {
 		if state.source != source && !overwrite {
 			// Registered by a different source, leave as-is.
 			return nil
diff --git a/agent/proxycfg/state.go b/agent/proxycfg/state.go
index d312c3b4c10cb..2347b04cc53b8 100644
--- a/agent/proxycfg/state.go
+++ b/agent/proxycfg/state.go
@@ -83,10 +83,20 @@ type state struct {
 	ch     chan UpdateEvent
 	snapCh chan ConfigSnapshot
 	reqCh  chan chan *ConfigSnapshot
+	doneCh chan struct{}
 
 	rateLimiter *rate.Limiter
 }
 
+func (s *state) stoppedRunning() bool {
+	select {
+	case <-s.doneCh:
+		return true
+	default:
+		return false
+	}
+}
+
 // failed returns whether run exited because a data source is in an
 // irrecoverable state.
 func (s *state) failed() bool {
@@ -182,6 +192,7 @@ func newState(id ProxyID, ns *structs.NodeService, source ProxySource, token str
 		ch:              ch,
 		snapCh:          make(chan ConfigSnapshot, 1),
 		reqCh:           make(chan chan *ConfigSnapshot, 1),
+		doneCh:          make(chan struct{}),
 		rateLimiter:     rateLimiter,
 	}, nil
 }
@@ -265,6 +276,9 @@ func (s *state) Watch() (<-chan ConfigSnapshot, error) {
 
 // Close discards the state and stops any long-running watches.
 func (s *state) Close(failed bool) error {
+	if s.stoppedRunning() {
+		return nil
+	}
 	if s.cancel != nil {
 		s.cancel()
 	}
@@ -314,6 +328,9 @@ func (s *state) run(ctx context.Context, snap *ConfigSnapshot) {
 }
 
 func (s *state) unsafeRun(ctx context.Context, snap *ConfigSnapshot) {
+	// Closing the done channel signals that this entire state is no longer
+	// going to be updated.
+	defer close(s.doneCh)
 	// Close the channel we return from Watch when we stop so consumers can stop
 	// watching and clean up their goroutines. It's important we do this here and
 	// not in Close since this routine sends on this chan and so might panic if it
@@ -429,9 +446,20 @@ func (s *state) unsafeRun(ctx context.Context, snap *ConfigSnapshot) {
 func (s *state) CurrentSnapshot() *ConfigSnapshot {
 	// Make a chan for the response to be sent on
 	ch := make(chan *ConfigSnapshot, 1)
-	s.reqCh <- ch
+
+	select {
+	case <-s.doneCh:
+		return nil
+	case s.reqCh <- ch:
+	}
+
 	// Wait for the response
-	return <-ch
+	select {
+	case <-s.doneCh:
+		return nil
+	case resp := <-ch:
+		return resp
+	}
 }
 
 // Changed returns whether or not the passed NodeService has had any of the