diff --git a/manager/dispatcher/dispatcher.go b/manager/dispatcher/dispatcher.go
index 12c2a81e34..7b9e175438 100644
--- a/manager/dispatcher/dispatcher.go
+++ b/manager/dispatcher/dispatcher.go
@@ -125,8 +125,17 @@ type clusterUpdate struct {
 
 // Dispatcher is responsible for dispatching tasks and tracking agent health.
 type Dispatcher struct {
-	mu                   sync.Mutex
-	wg                   sync.WaitGroup
+	// Mutex to synchronize access to dispatcher shared state e.g. nodes,
+	// lastSeenManagers, networkBootstrapKeys etc.
+	// TODO(anshul): This can potentially be removed and rpcRW used in its place.
+	mu sync.Mutex
+	// WaitGroup to handle the case when Stop() gets called before Run()
+	// has finished initializing the dispatcher.
+	wg sync.WaitGroup
+	// This RWMutex synchronizes RPC handlers and the dispatcher stop().
+	// The RPC handlers use the read lock while stop() uses the write lock
+	// and acts as a barrier to shutdown.
+	rpcRW                sync.RWMutex
 	nodes                *nodeStore
 	store                *store.MemoryStore
 	lastSeenManagers     []*api.WeightedPeer
@@ -318,7 +327,13 @@ func (d *Dispatcher) Stop() error {
 	d.cancel()
 	d.mu.Unlock()
 
+	// The active nodes list can be cleaned out only when all
+	// existing RPCs have finished.
+	// RPCs that start after rpcRW.Unlock() should find the context
+	// cancelled and should fail organically.
+	d.rpcRW.Lock()
 	d.nodes.Clean()
+	d.rpcRW.Unlock()
 
 	d.processUpdatesLock.Lock()
 	// In case there are any waiters. There is no chance of any starting
@@ -329,6 +344,11 @@ func (d *Dispatcher) Stop() error {
 
 	d.clusterUpdateQueue.Close()
 
+	// TODO(anshul): This use of Wait() could be unsafe.
+	// According to go's documentation on WaitGroup,
+	// Add() with a positive delta that occur when the counter is zero
+	// must happen before a Wait().
+	// As is, dispatcher Stop() can race with Run().
 	d.wg.Wait()
 
 	return nil
@@ -532,6 +552,14 @@ func (d *Dispatcher) register(ctx context.Context, nodeID string, description *a
 // UpdateTaskStatus updates status of task. Node should send such updates
 // on every status change of its tasks.
 func (d *Dispatcher) UpdateTaskStatus(ctx context.Context, r *api.UpdateTaskStatusRequest) (*api.UpdateTaskStatusResponse, error) {
+	d.rpcRW.RLock()
+	defer d.rpcRW.RUnlock()
+
+	dctx, err := d.isRunningLocked()
+	if err != nil {
+		return nil, err
+	}
+
 	nodeInfo, err := ca.RemoteNode(ctx)
 	if err != nil {
 		return nil, err
@@ -547,11 +575,6 @@ func (d *Dispatcher) UpdateTaskStatus(ctx context.Context, r *api.UpdateTaskStat
 	}
 	log := log.G(ctx).WithFields(fields)
 
-	dctx, err := d.isRunningLocked()
-	if err != nil {
-		return nil, err
-	}
-
 	if _, err := d.nodes.GetWithSession(nodeID, r.SessionID); err != nil {
 		return nil, err
 	}
@@ -723,16 +746,19 @@ func (d *Dispatcher) processUpdates(ctx context.Context) {
 // of tasks which should be run on node, if task is not present in that list,
 // it should be terminated.
 func (d *Dispatcher) Tasks(r *api.TasksRequest, stream api.Dispatcher_TasksServer) error {
-	nodeInfo, err := ca.RemoteNode(stream.Context())
+	d.rpcRW.RLock()
+	defer d.rpcRW.RUnlock()
+
+	dctx, err := d.isRunningLocked()
 	if err != nil {
 		return err
 	}
-	nodeID := nodeInfo.NodeID
 
-	dctx, err := d.isRunningLocked()
+	nodeInfo, err := ca.RemoteNode(stream.Context())
 	if err != nil {
 		return err
 	}
+	nodeID := nodeInfo.NodeID
 
 	fields := logrus.Fields{
 		"node.id":      nodeID,
@@ -846,16 +872,19 @@ func (d *Dispatcher) Tasks(r *api.TasksRequest, stream api.Dispatcher_TasksServe
 // Assignments is a stream of assignments for a node. Each message contains
 // either full list of tasks and secrets for the node, or an incremental update.
 func (d *Dispatcher) Assignments(r *api.AssignmentsRequest, stream api.Dispatcher_AssignmentsServer) error {
-	nodeInfo, err := ca.RemoteNode(stream.Context())
+	d.rpcRW.RLock()
+	defer d.rpcRW.RUnlock()
+
+	dctx, err := d.isRunningLocked()
 	if err != nil {
 		return err
 	}
-	nodeID := nodeInfo.NodeID
 
-	dctx, err := d.isRunningLocked()
+	nodeInfo, err := ca.RemoteNode(stream.Context())
 	if err != nil {
 		return err
 	}
+	nodeID := nodeInfo.NodeID
 
 	fields := logrus.Fields{
 		"node.id":      nodeID,
@@ -1103,6 +1132,17 @@ func (d *Dispatcher) markNodeNotReady(id string, state api.NodeStatus_State, mes
 // Node should send new heartbeat earlier than now + TTL, otherwise it will
 // be deregistered from dispatcher and its status will be updated to NodeStatus_DOWN
 func (d *Dispatcher) Heartbeat(ctx context.Context, r *api.HeartbeatRequest) (*api.HeartbeatResponse, error) {
+	d.rpcRW.RLock()
+	defer d.rpcRW.RUnlock()
+
+	// Its OK to call isRunning() here instead of isRunningLocked()
+	// because of the rpcRW readlock above.
+	// TODO(anshul) other uses of isRunningLocked() can probably
+	// also be removed.
+	if !d.isRunning() {
+		return nil, status.Errorf(codes.Aborted, "dispatcher is stopped")
+	}
+
 	nodeInfo, err := ca.RemoteNode(ctx)
 	if err != nil {
 		return nil, err
@@ -1137,17 +1177,21 @@ func (d *Dispatcher) getRootCACert() []byte {
 // a special boolean field Disconnect which if true indicates that node should
 // reconnect to another Manager immediately.
 func (d *Dispatcher) Session(r *api.SessionRequest, stream api.Dispatcher_SessionServer) error {
-	ctx := stream.Context()
-	nodeInfo, err := ca.RemoteNode(ctx)
+	d.rpcRW.RLock()
+	defer d.rpcRW.RUnlock()
+
+	dctx, err := d.isRunningLocked()
 	if err != nil {
 		return err
 	}
-	nodeID := nodeInfo.NodeID
 
-	dctx, err := d.isRunningLocked()
+	ctx := stream.Context()
+
+	nodeInfo, err := ca.RemoteNode(ctx)
 	if err != nil {
 		return err
 	}
+	nodeID := nodeInfo.NodeID
 
 	var sessionID string
 	if _, err := d.nodes.GetWithSession(nodeID, r.SessionID); err != nil {