diff --git a/spindle/config/config.go b/spindle/config/config.go
--- a/spindle/config/config.go
+++ b/spindle/config/config.go
@@ -62,7 +62,7 @@
 }
 
 type MicroVMPipelines struct {
-	ImageDir        string `env:"IMAGE_DIR, required"`
+	ImageDir        string `env:"IMAGE_DIR"`
 	OverlayDir      string `env:"OVERLAY_DIR, default="` // where microVM temporary disks will live
 	DefaultImage    string `env:"DEFAULT_IMAGE, default=nixos-x86_64"`
 	AgentPort       uint32 `env:"AGENT_PORT, default=10240"`
diff --git a/spindle/config/config_test.go b/spindle/config/config_test.go
new file mode 100644
--- /dev/null
+++ b/spindle/config/config_test.go
@@ -0,0 +1,20 @@
+package config
+
+import (
+	"context"
+	"testing"
+)
+
+func TestLoadAllowsUnconfiguredMicroVMEngine(t *testing.T) {
+	t.Setenv("SPINDLE_SERVER_HOSTNAME", "spindle.example.com")
+	t.Setenv("SPINDLE_SERVER_OWNER", "did:web:spindle.example.com")
+	t.Setenv("SPINDLE_MICROVM_PIPELINES_IMAGE_DIR", "")
+
+	cfg, err := Load(context.Background())
+	if err != nil {
+		t.Fatal(err)
+	}
+	if cfg.MicroVMPipelines.ImageDir != "" {
+		t.Fatalf("image directory = %q, want empty", cfg.MicroVMPipelines.ImageDir)
+	}
+}
diff --git a/spindle/engines/microvm/engine.go b/spindle/engines/microvm/engine.go
--- a/spindle/engines/microvm/engine.go
+++ b/spindle/engines/microvm/engine.go
@@ -46,6 +46,7 @@
 	l            *slog.Logger
 	cfg          *config.Config
 	db           *db.DB
+	agentMu      sync.Mutex
 	agent        *agentHub
 	scheduler    *engine.ResourceScheduler[Resources]
 	cgroupParent *CgroupParent
@@ -70,18 +71,11 @@
 
 func New(ctx context.Context, cfg *config.Config, d *db.DB) (*Engine, error) {
 	l := log.FromContext(ctx).With("component", "engine.microvm")
-	port := cfg.MicroVMPipelines.AgentPort
-	if port == 0 {
-		port = agentproto.DefaultPort
-	}
-	agent, err := newAgentHub(port, l)
-	if err != nil {
-		return nil, err
-	}
 	budget, max, agingThreshold := newVMBudgetConfig(cfg.MicroVMPipelines)
 	l.Info("initialized microVM workflow budget", "budget", budget.String(), "maxWorkflow", max.String(), "agingThreshold", agingThreshold)
 
 	var cgroupParent *CgroupParent
+	var err error
 	if cfg.MicroVMPipelines.EnableCgroups {
 		cgroupParent, err = initCgroupParent(cfg.MicroVMPipelines.CgroupParent, cfg.MicroVMPipelines.CgroupSupervisorMemoryMinMiB, l)
 		if err != nil {
@@ -93,11 +87,30 @@
 		l:            l,
 		cfg:          cfg,
 		db:           d,
-		agent:        agent,
 		scheduler:    engine.NewResourceScheduler(budget, max, agingThreshold),
 		cgroupParent: cgroupParent,
 		cleanup:      make(map[string][]cleanupFunc),
 	}, nil
+}
+
+func (e *Engine) ensureAgentHub() (*agentHub, error) {
+	e.agentMu.Lock()
+	defer e.agentMu.Unlock()
+
+	if e.agent != nil {
+		return e.agent, nil
+	}
+
+	port := e.cfg.MicroVMPipelines.AgentPort
+	if port == 0 {
+		port = agentproto.DefaultPort
+	}
+	agent, err := newAgentHub(port, e.l)
+	if err != nil {
+		return nil, err
+	}
+	e.agent = agent
+	return agent, nil
 }
 
 func (e *Engine) InitWorkflow(twf tangled.Pipeline_Workflow, tpl tangled.Pipeline) (*models.Workflow, error) {
@@ -210,7 +223,11 @@
 	if err != nil {
 		return err
 	}
-	connCh, unregister, err := e.agent.expect(cid)
+	agent, err := e.ensureAgentHub()
+	if err != nil {
+		return err
+	}
+	connCh, unregister, err := agent.expect(cid)
 	if err != nil {
 		return err
 	}
diff --git a/spindle/engines/microvm/engine_test.go b/spindle/engines/microvm/engine_test.go
--- a/spindle/engines/microvm/engine_test.go
+++ b/spindle/engines/microvm/engine_test.go
@@ -1,6 +1,7 @@
 package microvm
 
 import (
+	"context"
 	"encoding/json"
 	"log/slog"
 	"os"
@@ -33,6 +34,16 @@
 				DefaultImage: "alpine",
 			},
 		},
+	}
+}
+
+func TestNewDefersAgentHubUntilWorkflowSetup(t *testing.T) {
+	e, err := New(context.Background(), &config.Config{}, nil)
+	if err != nil {
+		t.Fatal(err)
+	}
+	if e.agent != nil {
+		t.Fatal("agent hub started during engine initialization")
 	}
 }
 
diff --git a/spindle/engines/microvm/image.go b/spindle/engines/microvm/image.go
--- a/spindle/engines/microvm/image.go
+++ b/spindle/engines/microvm/image.go
@@ -181,7 +181,12 @@
 		return ImageSpec{}, "", "", fmt.Errorf("invalid microVM image name %q: must be a plain name, not a path", name)
 	}
 
-	candidates := imageCandidates(e.cfg.MicroVMPipelines.ImageDir, name)
+	imageDir := strings.TrimSpace(e.cfg.MicroVMPipelines.ImageDir)
+	if imageDir == "" {
+		return ImageSpec{}, "", "", fmt.Errorf("microVM workflows require SPINDLE_MICROVM_PIPELINES_IMAGE_DIR")
+	}
+
+	candidates := imageCandidates(imageDir, name)
 	for _, candidate := range candidates {
 		path, ok, err := imageSpecPath(candidate)
 		if err != nil {
diff --git a/spindle/engines/microvm/image_test.go b/spindle/engines/microvm/image_test.go
--- a/spindle/engines/microvm/image_test.go
+++ b/spindle/engines/microvm/image_test.go
@@ -77,6 +77,14 @@
 	}
 }
 
+func TestResolveImageRequiresImageDirOnlyWhenUsed(t *testing.T) {
+	e := testEngine(t, "")
+	_, _, _, err := e.resolveImage("nixos")
+	if err == nil || !strings.Contains(err.Error(), "SPINDLE_MICROVM_PIPELINES_IMAGE_DIR") {
+		t.Fatalf("missing image directory should error when resolving an image, got: %v", err)
+	}
+}
+
 func TestResolveImageRejectsPaths(t *testing.T) {
 	e := testEngine(t, t.TempDir())
 	for _, name := range []string{"/etc/passwd", "../evil", "sub/evil", "..", "."} {