diff --git a/lib/instances/manager.go b/lib/instances/manager.go
index 1a2215c0..71bb75b4 100644
--- a/lib/instances/manager.go
+++ b/lib/instances/manager.go
@@ -226,9 +226,21 @@ func NewManagerWithConfig(p *paths.Paths, imageManager images.Manager, systemMan
 		logger.FromContext(context.Background()).WarnContext(context.Background(), "failed to recover pending standby compression jobs", "error", err)
 	}
 
+	// Heal any drift between the templates registry and on-disk
+	// instances after a crash or out-of-band fork delete.
+	if err := m.reconcileTemplateState(context.Background()); err != nil {
+		logger.FromContext(context.Background()).WarnContext(context.Background(), "failed to reconcile template state at boot", "error", err)
+	}
+
 	return m
 }
 
+// ReconcileTemplateState heals registry/instances drift on demand. Useful
+// for tests and for periodic GC tickers driven by the host process.
+func (m *manager) ReconcileTemplateState(ctx context.Context) error {
+	return m.reconcileTemplateState(ctx)
+}
+
 // SetResourceValidator sets the resource validator for aggregate limit checking.
 // This is called after initialization to avoid circular dependencies.
 func (m *manager) SetResourceValidator(v ResourceValidator) {
diff --git a/lib/instances/storage.go b/lib/instances/storage.go
index f290298c..73eaf6d6 100644
--- a/lib/instances/storage.go
+++ b/lib/instances/storage.go
@@ -77,6 +77,21 @@ func (m *manager) loadMetadata(id string) (*metadata, error) {
 	return &meta, nil
 }
 
+// loadMetadataFromFile reads a metadata file by path. Used by sweepers
+// that already have the path from listMetadataFiles and don't want to
+// reverse-derive an instance id.
+func loadMetadataFromFile(path string) (*metadata, error) {
+	data, err := os.ReadFile(path)
+	if err != nil {
+		return nil, fmt.Errorf("read metadata: %w", err)
+	}
+	var meta metadata
+	if err := json.Unmarshal(data, &meta); err != nil {
+		return nil, fmt.Errorf("unmarshal metadata: %w", err)
+	}
+	return &meta, nil
+}
+
 // saveMetadata saves instance metadata to disk
 func (m *manager) saveMetadata(meta *metadata) error {
 	metaPath := m.paths.InstanceMetadata(meta.Id)
diff --git a/lib/instances/templates.go b/lib/instances/templates.go
index 91383615..e5f00a42 100644
--- a/lib/instances/templates.go
+++ b/lib/instances/templates.go
@@ -316,3 +316,68 @@ func (m *manager) dropTemplateForkRefcount(ctx context.Context, templateID strin
 			"template_id", templateID, "error", err)
 	}
 }
+
+// reconcileTemplateState heals drift between the templates registry and
+// the instances directory. It rewrites ForkCount on every template using
+// the actual ForkOfTemplate population on disk, and removes registry
+// entries whose source instance no longer exists. Safe to call at boot
+// and on a periodic GC tick. Bestow the work on a background goroutine
+// when the cost matters; this method is synchronous and modest.
+func (m *manager) reconcileTemplateState(ctx context.Context) error {
+	if m.templateRegistry == nil {
+		return nil
+	}
+	log := logger.FromContext(ctx)
+
+	metaFiles, err := m.listMetadataFiles()
+	if err != nil {
+		return fmt.Errorf("list instance metadata for template GC: %w", err)
+	}
+
+	observedForks := make(map[string]int)
+	templateSourceInstances := make(map[string]struct{})
+	for _, path := range metaFiles {
+		meta, err := loadMetadataFromFile(path)
+		if err != nil {
+			log.WarnContext(ctx, "skip metadata during template GC", "path", path, "error", err)
+			continue
+		}
+		stored := meta.StoredMetadata
+		if stored.ForkOfTemplate != "" {
+			observedForks[stored.ForkOfTemplate]++
+		}
+		if stored.IsTemplate {
+			templateSourceInstances[stored.Id] = struct{}{}
+		}
+	}
+
+	if err := m.templateRegistry.Reconcile(ctx, observedForks); err != nil {
+		return fmt.Errorf("reconcile template fork counts: %w", err)
+	}
+
+	all, err := m.templateRegistry.List(ctx, nil)
+	if err != nil {
+		return fmt.Errorf("list templates for orphan sweep: %w", err)
+	}
+	for _, tpl := range all {
+		if _, ok := templateSourceInstances[tpl.SourceInstanceID]; ok {
+			continue
+		}
+		if tpl.ForkCount > 0 {
+			// Source gone but forks still reference the template; leave
+			// the registry entry so future fork GC can find it. The
+			// underlying mem-file is still alive on disk because forks
+			// hold open file descriptors via the symlink.
+			log.WarnContext(ctx, "template has live forks but no source instance",
+				"template_id", tpl.ID, "fork_count", tpl.ForkCount)
+			continue
+		}
+		log.InfoContext(ctx, "deleting orphaned template registry entry",
+			"template_id", tpl.ID, "source_instance_id", tpl.SourceInstanceID)
+		if err := m.templateRegistry.Delete(ctx, tpl.ID); err != nil {
+			log.WarnContext(ctx, "failed to delete orphaned template",
+				"template_id", tpl.ID, "error", err)
+		}
+	}
+	return nil
+}
diff --git a/lib/templates/registry.go b/lib/templates/registry.go
index fed3f169..0cb2cb9c 100644
--- a/lib/templates/registry.go
+++ b/lib/templates/registry.go
@@ -45,6 +45,13 @@ type Registry interface {
 	// template (floor 0). Used when a fork is deleted. Touching
 	// templates that were already deleted is a no-op.
 	DecrementForkCount(ctx context.Context, id string) (*Template, error)
+
+	// Reconcile walks the registry and rewrites ForkCount on every
+	// template using observedForks: the count of live forks per
+	// template id. Templates not present in observedForks fall to
+	// zero. Used to heal drift after a crash, an out-of-band fork
+	// delete, or any other path that bypassed Increment/Decrement.
+	Reconcile(ctx context.Context, observedForks map[string]int) error
 }
 
 // ListFilter narrows the templates returned by Registry.List.
@@ -231,6 +238,34 @@ func (r *FileRegistry) IncrementForkCount(ctx context.Context, id string) (*Temp
 	return t, nil
 }
 
+// Reconcile rewrites ForkCount on every persisted template using
+// observedForks as the authority. Templates not present in observedForks
+// are treated as having zero live forks. Errors on individual templates
+// are returned as a wrapped multi-error so the caller can decide whether
+// to treat partial reconciliation as fatal; reconciliation is best-effort
+// and never deletes templates by itself.
+func (r *FileRegistry) Reconcile(ctx context.Context, observedForks map[string]int) error {
+	_ = ctx
+	r.mu.Lock()
+	defer r.mu.Unlock()
+	all, err := r.listLocked()
+	if err != nil {
+		return err
+	}
+	var firstErr error
+	for _, t := range all {
+		want := observedForks[t.ID]
+		if t.ForkCount == want {
+			continue
+		}
+		t.ForkCount = want
+		if err := r.writeLocked(t); err != nil && firstErr == nil {
+			firstErr = fmt.Errorf("reconcile template %s: %w", t.ID, err)
+		}
+	}
+	return firstErr
+}
+
 func (r *FileRegistry) DecrementForkCount(ctx context.Context, id string) (*Template, error) {
 	_ = ctx
 	r.mu.Lock()
diff --git a/lib/templates/registry_test.go b/lib/templates/registry_test.go
index 79a93031..164fe13d 100644
--- a/lib/templates/registry_test.go
+++ b/lib/templates/registry_test.go
@@ -123,3 +123,32 @@ func TestFileRegistry_SaveValidates(t *testing.T) {
 	err := r.Save(context.Background(), &Template{Name: "x"})
 	assert.True(t, errors.Is(err, ErrInvalid))
 }
+
+func TestFileRegistry_Reconcile(t *testing.T) {
+	r := newTestRegistry(t)
+	a := sampleTemplate("a", "alpha")
+	a.ForkCount = 5
+	b := sampleTemplate("b", "beta")
+	b.ForkCount = 0
+	c := sampleTemplate("c", "gamma")
+	c.ForkCount = 7
+	require.NoError(t, r.Save(context.Background(), a))
+	require.NoError(t, r.Save(context.Background(), b))
+	require.NoError(t, r.Save(context.Background(), c))
+
+	require.NoError(t, r.Reconcile(context.Background(), map[string]int{
+		"a": 2,
+		"b": 3,
+		// c omitted -> should fall to 0
+	}))
+
+	got, err := r.Get(context.Background(), "a")
+	require.NoError(t, err)
+	assert.Equal(t, 2, got.ForkCount)
+	got, err = r.Get(context.Background(), "b")
+	require.NoError(t, err)
+	assert.Equal(t, 3, got.ForkCount)
+	got, err = r.Get(context.Background(), "c")
+	require.NoError(t, err)
+	assert.Equal(t, 0, got.ForkCount)
+}