diff --git a/fleetspeak/src/client/https/polling.go b/fleetspeak/src/client/https/polling.go
index 53a332a2..d194cd62 100644
--- a/fleetspeak/src/client/https/polling.go
+++ b/fleetspeak/src/client/https/polling.go
@@ -59,15 +59,19 @@ type Communicator struct {
 
 	certBytes []byte
 
-	wakeUp       chan struct{}
-	pollComplete chan error
-	mu           sync.Mutex
-	pollCancel   context.CancelFunc
+	// Synchronization for Reset/Flush
+	wakeUp      chan struct{}
+	mu          sync.Mutex
+	pollDone    chan struct{}
+	lastPollErr error
+	pollCancel  context.CancelFunc
 }
 
 // Setup implements comms.Communicator.
 func (c *Communicator) Setup(cl comms.Context) error {
 	c.cctx = cl
+	c.pollDone = make(chan struct{})
+	close(c.pollDone) // Start closed so Flush returns immediately if no messages.
 	return c.configure()
 }
 
@@ -114,7 +118,6 @@ func (c *Communicator) configure() error {
 	c.ctx, c.done = context.WithCancel(context.Background())
 	c.clientCertificateHeader = si.ClientCertificateHeader
 	c.wakeUp = make(chan struct{}, 1)
-	c.pollComplete = make(chan error, 1)
 	c.certBytes = certBytes
 	return nil
 }
@@ -141,13 +144,9 @@ func (c *Communicator) Reset() {
 	if c.pollCancel != nil {
 		c.pollCancel()
 	}
+	c.pollDone = make(chan struct{})
 	c.mu.Unlock()
 	c.hc.Transport.(*http.Transport).CloseIdleConnections()
-	// Drain pollComplete to ensure Flush waits for a new poll.
-	select {
-	case <-c.pollComplete:
-	default:
-	}
 	select {
 	case c.wakeUp <- struct{}{}:
 	default:
@@ -158,10 +157,23 @@ func (c *Communicator) Reset() {
 func (c *Communicator) Flush(ctx context.Context) error {
 	log.InfoContextf(ctx, "Flush called")
 	for {
+		c.mu.Lock()
+		done := c.pollDone
+		c.mu.Unlock()
+
 		select {
 		case <-ctx.Done():
 			return ctx.Err()
-		case err := <-c.pollComplete:
+		case <-c.ctx.Done():
+			return c.ctx.Err()
+		case <-done:
+			c.mu.Lock()
+			err := c.lastPollErr
+			if err != nil && c.pollDone != done {
+				c.mu.Unlock()
+				continue
+			}
+			c.mu.Unlock()
 			return err
 		}
 	}
@@ -193,25 +205,48 @@ func (c *Communicator) processingLoop() {
 	// for the MinFailureDelay.
 	poll := func() {
 		var err error
+		c.mu.Lock()
+		select {
+		case <-c.pollDone:
+			c.pollDone = make(chan struct{})
+		default:
+		}
+		reqCtx, cancel := context.WithCancel(c.ctx)
+		c.pollCancel = cancel
+		myDone := c.pollDone
+		c.mu.Unlock()
+
 		defer func() {
-			select {
-			case c.pollComplete <- err:
-			default:
-			}
+			cancel()
+			c.mu.Lock()
+			c.pollCancel = nil
+			c.lastPollErr = err
+			close(myDone)
+			c.mu.Unlock()
 		}()
+
 		c.wd.Reset()
 		if c.cctx.CurrentID() != c.id {
 			c.configure()
 		}
 		var active bool
-		active, err = c.poll(toSend)
+		active, err = c.poll(reqCtx, toSend)
 		if err != nil {
+			c.mu.Lock()
+			wasReset := errors.Is(err, context.Canceled) && c.ctx.Err() == nil
+			c.mu.Unlock()
+
+			if wasReset {
+				return
+			}
+
 			log.Warningf("Failure during polling: %v", err)
 			for _, m := range toSend {
 				m.Nack()
 			}
 			toSend = nil
 			toSendSize = 0
+			oldestUnsent = time.Time{}
 
 			if (!lastPoll.IsZero()) && (time.Since(lastPoll) > time.Duration(c.conf.FailureSuicideTimeSeconds)*time.Second) {
 				// Die in the hopes that our replacement will be better configured, or otherwise have better luck.
@@ -310,6 +345,14 @@ func (c *Communicator) processingLoop() {
 			poll()
 		case m := <-c.cctx.Outbox():
 			t.Stop()
+			c.mu.Lock()
+			select {
+			case <-c.pollDone:
+				c.pollDone = make(chan struct{})
+			default:
+			}
+			c.mu.Unlock()
+
 			toSend = append(toSend, m)
 			toSendSize += 2 + proto.Size(m.M)
 			if toSendSize >= sendBytesThreshold ||
@@ -324,7 +367,7 @@ func (c *Communicator) processingLoop() {
 	}
 }
 
-func (c *Communicator) poll(toSend []comms.MessageInfo) (bool, error) {
+func (c *Communicator) poll(ctx context.Context, toSend []comms.MessageInfo) (bool, error) {
 	var sent bool // records whether an interesting (non-LOW) priority message was sent.
 	msgs := make([]*fspb.Message, 0, len(toSend))
 	for _, m := range toSend {
@@ -347,9 +390,12 @@ func (c *Communicator) poll(toSend []comms.MessageInfo) (bool, error) {
 	}
 
 	for i, host := range c.hosts {
-		cd, err := c.pollHost(host, data)
+		cd, err := c.pollHost(ctx, host, data)
 		if err != nil {
 			log.Warningf("Error polling %q for ContactData: %v", host, err)
+			if ctx.Err() != nil {
+				return false, ctx.Err()
+			}
 			continue
 		}
 		if i != 0 {
@@ -367,7 +413,7 @@ func (c *Communicator) poll(toSend []comms.MessageInfo) (bool, error) {
 	return false, errors.New("unable to contact any server")
 }
 
-func (c *Communicator) pollHost(host string, data []byte) (*fspb.ContactData, error) {
+func (c *Communicator) pollHost(ctx context.Context, host string, data []byte) (*fspb.ContactData, error) {
 	var sendErr, recvErr error
 	var sendSize, recvSize int
 	defer func() {
@@ -396,17 +442,7 @@ func (c *Communicator) pollHost(host string, data []byte) (*fspb.ContactData, er
 	if sendErr != nil {
 		return nil, sendErr
 	}
-	var reqCtx context.Context
-	c.mu.Lock()
-	reqCtx, c.pollCancel = context.WithCancel(c.ctx)
-	c.mu.Unlock()
-	defer func() {
-		c.mu.Lock()
-		c.pollCancel()
-		c.pollCancel = nil
-		c.mu.Unlock()
-	}()
-	req = req.WithContext(reqCtx)
+	req = req.WithContext(ctx)
 	SetContentEncoding(req.Header, c.conf.GetCompression())
 	if c.clientCertificateHeader != "" {
 		bc := pem.EncodeToMemory(&pem.Block{Type: "CERTIFICATE", Bytes: c.certBytes})