diff --git a/internal/pkg/api/handleCheckin.go b/internal/pkg/api/handleCheckin.go
index 8512a637c1..5ad76b8fec 100644
--- a/internal/pkg/api/handleCheckin.go
+++ b/internal/pkg/api/handleCheckin.go
@@ -302,7 +302,16 @@ func (ct *CheckinT) ProcessRequest(zlog zerolog.Logger, w http.ResponseWriter, r
 		for {
 			select {
 			case <-ctx.Done():
-				span.End()
+				defer span.End()
+				// If the request context is canceled, the API server is shutting down.
+				// We want to immediatly stop the long-poll and return a 200 with the ackToken and no actions.
+				if errors.Is(ctx.Err(), context.Canceled) {
+					resp := CheckinResponse{
+						AckToken: &ackToken,
+						Action:   "checkin",
+					}
+					return ct.writeResponse(zlog, w, r, agent, resp)
+				}
 				return ctx.Err()
 			case acdocs := <-actCh:
 				var acs []Action
diff --git a/internal/pkg/api/handleStatus.go b/internal/pkg/api/handleStatus.go
index 5875dfe4be..b17711aeb1 100644
--- a/internal/pkg/api/handleStatus.go
+++ b/internal/pkg/api/handleStatus.go
@@ -91,6 +91,12 @@ func (st StatusT) handleStatus(zlog zerolog.Logger, sm policy.SelfMonitor, bi bu
 	span, _ = apm.StartSpan(r.Context(), "response", "write")
 	defer span.End()
 
+	// If the request context has been cancelled, such as the case when the server is stopping we should return a 503
+	// Note that the API server uses Shutdown, so no new requests should be accepted and this edge case will be rare.
+	if errors.Is(r.Context().Err(), context.Canceled) {
+		state = client.UnitStateStopping
+	}
+
 	data, err := json.Marshal(&resp)
 	if err != nil {
 		return err
diff --git a/internal/pkg/api/server.go b/internal/pkg/api/server.go
index 4b3e4e9da5..f2bf4d7939 100644
--- a/internal/pkg/api/server.go
+++ b/internal/pkg/api/server.go
@@ -8,6 +8,7 @@ import (
 	"context"
 	"crypto/tls"
 	"errors"
+	"fmt"
 	slog "log"
 	"net"
 	"net/http"
@@ -75,25 +76,7 @@ func (s *server) Run(ctx context.Context) error {
 		ConnState:         diagConn,
 	}
 
-	forceCh := make(chan struct{})
-	defer close(forceCh)
-
-	// handler to close server
-	go func() {
-		select {
-		case <-ctx.Done():
-			zerolog.Ctx(ctx).Debug().Msg("force server close on ctx.Done()")
-			err := srv.Close()
-			if err != nil {
-				zerolog.Ctx(ctx).Error().Err(err).Msg("error while closing server")
-			}
-		case <-forceCh:
-			zerolog.Ctx(ctx).Debug().Msg("go routine forced closed on exit")
-		}
-	}()
-
 	var listenCfg net.ListenConfig
-
 	ln, err := listenCfg.Listen(ctx, "tcp", s.addr)
 	if err != nil {
 		return err
@@ -130,23 +113,27 @@ func (s *server) Run(ctx context.Context) error {
 		zerolog.Ctx(ctx).Warn().Msg("Exposed over insecure HTTP; enablement of TLS is strongly recommended")
 	}
 
+	// Start the API server on another goroutine and return any non ErrServerClosed errors through a channel.
 	errCh := make(chan error)
-	baseCtx, cancel := context.WithCancel(ctx)
-	defer cancel()
-
 	go func(ctx context.Context, errCh chan error, ln net.Listener) {
 		zerolog.Ctx(ctx).Info().Msgf("Listening on %s", s.addr)
 		if err := srv.Serve(ln); err != nil && !errors.Is(err, http.ErrServerClosed) {
 			errCh <- err
 		}
-	}(baseCtx, errCh, ln)
+	}(ctx, errCh, ln)
 
 	select {
+	// Listen and return any errors that occur from the server listener
 	case err := <-errCh:
 		if !errors.Is(err, context.Canceled) {
-			return err
+			return fmt.Errorf("error while serving API listener: %w", err)
+		}
+	// Do a clean shutdown if the context is cancelled
+	// Note that is will wait for connections to close, we may want to use a new timeout value here.
+	case <-ctx.Done():
+		if err := srv.Shutdown(context.TODO()); err != nil {
+			return fmt.Errorf("error while shutting down api listener: %w", err)
 		}
-	case <-baseCtx.Done():
 	}
 
 	return nil
diff --git a/internal/pkg/checkin/bulk.go b/internal/pkg/checkin/bulk.go
index cab3caf3f2..c097e3e4ba 100644
--- a/internal/pkg/checkin/bulk.go
+++ b/internal/pkg/checkin/bulk.go
@@ -99,6 +99,7 @@ func (bc *Bulk) timestamp() string {
 
 // CheckIn will add the agent (identified by id) to the pending set.
 // The pending agents are sent to elasticsearch as a bulk update at each flush interval.
+// NOTE: If Checkin is called after Run has returned it will just add the entry to the pending map and not do any operations, this may occur when the fleet-server is shutting down.
 // WARNING: Bulk will take ownership of fields, so do not use after passing in.
 func (bc *Bulk) CheckIn(id string, status string, message string, meta []byte, components []byte, seqno sqn.SeqNo, newVer string) error {
 	// Separate out the extra data to minimize
diff --git a/internal/pkg/server/fleet.go b/internal/pkg/server/fleet.go
index 95b08b9b7e..8100bb681a 100644
--- a/internal/pkg/server/fleet.go
+++ b/internal/pkg/server/fleet.go
@@ -205,6 +205,8 @@ LOOP:
 		}
 	}
 
+	// FIXME cancelling the context will break out of the above loop and wait 1s, we should instead have a cancel context or some way to ensure that the API servers have shut down correctly.
+
 	// Server is coming down; wait for the server group to exit cleanly.
 	// Timeout if something is locked up.
 	err = safeWait(srvEg, time.Second)
@@ -376,6 +378,7 @@ func (f *Fleet) runServer(ctx context.Context, cfg *config.Config) (err error) {
 	// unexpectedly (ie. not cancelled by the bulkCancel context).
 	errCh := make(chan error)
 
+	// FIXME why not run this in the errgroup?
 	go func() {
 		runFunc := loggedRunFunc(bulkCtx, "Bulker", bulker.Run)
 
@@ -505,10 +508,10 @@ func (f *Fleet) runSubsystems(ctx context.Context, cfg *config.Config, g *errgro
 	if err != nil {
 		return err
 	}
-	g.Go(loggedRunFunc(ctx, "Revision monitor", am.Run))
+	g.Go(loggedRunFunc(ctx, "Action monitor", am.Run))
 
 	ad = action.NewDispatcher(am, cfg.Inputs[0].Server.Limits.ActionLimit.Interval, cfg.Inputs[0].Server.Limits.ActionLimit.Burst)
-	g.Go(loggedRunFunc(ctx, "Revision dispatcher", ad.Run))
+	g.Go(loggedRunFunc(ctx, "Action dispatcher", ad.Run))
 	tr, err = action.NewTokenResolver(bulker)
 	if err != nil {
 		return err