diff --git a/CHANGELOG.md b/CHANGELOG.md
index 19ed22f15989..4f0fd0abc446 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -29,6 +29,9 @@ Main (unreleased)
 
 - Fixed an issue where `loki.process` validation for stage `metric.counter` was 
   allowing invalid combination of configuration options. (@thampiotr)
+
+- Fixed issue where adding a module after initial start, that failed to load then subsequently resolving the issue would cause the module to
+  permanently fail to load with `id already exists` error. (@mattdurham)
   
 ### Enhancements
 
diff --git a/component/module/module.go b/component/module/module.go
index 79d95a002826..53e886721e65 100644
--- a/component/module/module.go
+++ b/component/module/module.go
@@ -7,6 +7,7 @@ import (
 	"sync"
 	"time"
 
+	"github.com/go-kit/log/level"
 	"github.com/grafana/agent/component"
 )
 
@@ -71,7 +72,10 @@ func (c *ModuleComponent) LoadFlowSource(args map[string]any, contentValue strin
 
 // RunFlowController runs the flow controller that all module components start.
 func (c *ModuleComponent) RunFlowController(ctx context.Context) {
-	c.mod.Run(ctx)
+	err := c.mod.Run(ctx)
+	if err != nil {
+		level.Error(c.opts.Logger).Log("msg", "error running module", "id", c.opts.ID, "err", err)
+	}
 }
 
 // CurrentHealth contains the implementation details for CurrentHealth in a module component.
diff --git a/component/registry.go b/component/registry.go
index f544bf8287f7..20a364be81c4 100644
--- a/component/registry.go
+++ b/component/registry.go
@@ -49,7 +49,7 @@ type Module interface {
 	//
 	// Run blocks until the provided context is canceled. The ID of a module as defined in
 	// ModuleController.NewModule will not be released until Run returns.
-	Run(context.Context)
+	Run(context.Context) error
 }
 
 // ExportFunc is used for onExport of the Module
diff --git a/pkg/flow/componenttest/testfailmodule.go b/pkg/flow/componenttest/testfailmodule.go
new file mode 100644
index 000000000000..011659f95564
--- /dev/null
+++ b/pkg/flow/componenttest/testfailmodule.go
@@ -0,0 +1,67 @@
+package componenttest
+
+import (
+	"context"
+	"fmt"
+
+	"github.com/grafana/agent/component"
+	mod "github.com/grafana/agent/component/module"
+)
+
+func init() {
+	component.Register(component.Registration{
+		Name:    "test.fail.module",
+		Args:    TestFailArguments{},
+		Exports: mod.Exports{},
+
+		Build: func(opts component.Options, args component.Arguments) (component.Component, error) {
+			m, err := mod.NewModuleComponent(opts)
+			if err != nil {
+				return nil, err
+			}
+			if args.(TestFailArguments).Fail {
+				return nil, fmt.Errorf("module told to fail")
+			}
+			err = m.LoadFlowSource(nil, args.(TestFailArguments).Content)
+			if err != nil {
+				return nil, err
+			}
+			return &TestFailModule{
+				mc:      m,
+				content: args.(TestFailArguments).Content,
+				opts:    opts,
+				fail:    args.(TestFailArguments).Fail,
+				ch:      make(chan error),
+			}, nil
+		},
+	})
+}
+
+type TestFailArguments struct {
+	Content string `river:"content,attr"`
+	Fail    bool   `river:"fail,attr,optional"`
+}
+
+type TestFailModule struct {
+	content string
+	opts    component.Options
+	ch      chan error
+	mc      *mod.ModuleComponent
+	fail    bool
+}
+
+func (t *TestFailModule) Run(ctx context.Context) error {
+	go t.mc.RunFlowController(ctx)
+	<-ctx.Done()
+	return nil
+}
+
+func (t *TestFailModule) UpdateContent(content string) error {
+	t.content = content
+	err := t.mc.LoadFlowSource(nil, t.content)
+	return err
+}
+
+func (t *TestFailModule) Update(_ component.Arguments) error {
+	return nil
+}
diff --git a/pkg/flow/flow_services_test.go b/pkg/flow/flow_services_test.go
index 128b1267e180..7639daea8144 100644
--- a/pkg/flow/flow_services_test.go
+++ b/pkg/flow/flow_services_test.go
@@ -183,7 +183,7 @@ func TestFlow_GetServiceConsumers_Modules(t *testing.T) {
 	ctx, cancel := context.WithCancel(context.Background())
 	defer cancel()
 
-	componentBuilt := util.NewWaitTrigger()
+	componentRunning := util.NewWaitTrigger()
 
 	var (
 		svc = &testservices.Fake{
@@ -218,9 +218,14 @@ func TestFlow_GetServiceConsumers_Modules(t *testing.T) {
 				Name:          "service_consumer",
 				Args:          struct{}{},
 				NeedsServices: []string{"service"},
-				Build: func(_ component.Options, _ component.Arguments) (component.Component, error) {
-					componentBuilt.Trigger()
-					return &testcomponents.Fake{}, nil
+				Build: func(o component.Options, _ component.Arguments) (component.Component, error) {
+					return &testcomponents.Fake{
+						RunFunc: func(ctx context.Context) error {
+							componentRunning.Trigger()
+							<-ctx.Done()
+							return nil
+						},
+					}, nil
 				},
 			},
 		}
@@ -243,7 +248,7 @@ func TestFlow_GetServiceConsumers_Modules(t *testing.T) {
 	require.NoError(t, ctrl.LoadSource(f, nil))
 	go ctrl.Run(ctx)
 
-	require.NoError(t, componentBuilt.Wait(5*time.Second), "Component should have been built")
+	require.NoError(t, componentRunning.Wait(5*time.Second), "Component should have been built")
 
 	consumers := ctrl.GetServiceConsumers("service")
 	require.Len(t, consumers, 2, "There should be a consumer for the module loader and the module's component")
diff --git a/pkg/flow/internal/controller/loader_test.go b/pkg/flow/internal/controller/loader_test.go
index 2351218d642b..c6b491f4c899 100644
--- a/pkg/flow/internal/controller/loader_test.go
+++ b/pkg/flow/internal/controller/loader_test.go
@@ -6,6 +6,7 @@ import (
 	"strings"
 	"testing"
 
+	"github.com/grafana/agent/component"
 	"github.com/grafana/agent/pkg/flow/internal/controller"
 	"github.com/grafana/agent/pkg/flow/internal/dag"
 	"github.com/grafana/agent/pkg/flow/logging"
@@ -209,7 +210,7 @@ func TestScopeWithFailingComponent(t *testing.T) {
 				OnComponentUpdate: func(cn *controller.ComponentNode) { /* no-op */ },
 				Registerer:        prometheus.NewRegistry(),
 				NewModuleController: func(id string, availableServices []string) controller.ModuleController {
-					return nil
+					return fakeModuleController{}
 				},
 			},
 		}
@@ -304,3 +305,16 @@ func requireGraph(t *testing.T, g *dag.Graph, expect graphDefinition) {
 	}
 	require.ElementsMatch(t, expect.OutEdges, actualEdges, "List of edges do not match")
 }
+
+type fakeModuleController struct{}
+
+func (f fakeModuleController) NewModule(id string, export component.ExportFunc) (component.Module, error) {
+	return nil, nil
+}
+
+func (f fakeModuleController) ModuleIDs() []string {
+	return nil
+}
+
+func (f fakeModuleController) ClearModuleIDs() {
+}
diff --git a/pkg/flow/internal/controller/node_component.go b/pkg/flow/internal/controller/node_component.go
index cab7109141a0..9481fd1f5b5b 100644
--- a/pkg/flow/internal/controller/node_component.go
+++ b/pkg/flow/internal/controller/node_component.go
@@ -257,7 +257,6 @@ func (cn *ComponentNode) Evaluate(scope *vm.Scope) error {
 		msg := fmt.Sprintf("component evaluation failed: %s", err)
 		cn.setEvalHealth(component.HealthTypeUnhealthy, msg)
 	}
-
 	return err
 }
 
@@ -303,7 +302,7 @@ func (cn *ComponentNode) evaluate(scope *vm.Scope) error {
 }
 
 // Run runs the managed component in the calling goroutine until ctx is
-// canceled. Evaluate must have been called at least once without retuning an
+// canceled. Evaluate must have been called at least once without returning an
 // error before calling Run.
 //
 // Run will immediately return ErrUnevaluated if Evaluate has never been called
diff --git a/pkg/flow/module.go b/pkg/flow/module.go
index f0687b8873a7..10aa353ee882 100644
--- a/pkg/flow/module.go
+++ b/pkg/flow/module.go
@@ -6,6 +6,7 @@ import (
 	"path"
 	"sync"
 
+	"github.com/go-kit/log/level"
 	"github.com/grafana/agent/component"
 	"github.com/grafana/agent/pkg/flow/internal/controller"
 	"github.com/grafana/agent/pkg/flow/internal/worker"
@@ -46,9 +47,6 @@ func (m *moduleController) NewModule(id string, export component.ExportFunc) (co
 	if id != "" {
 		fullPath = path.Join(fullPath, id)
 	}
-	if _, found := m.modules[fullPath]; found {
-		return nil, fmt.Errorf("id %s already exists", id)
-	}
 
 	mod := newModule(&moduleOptions{
 		ID:                      fullPath,
@@ -57,26 +55,33 @@ func (m *moduleController) NewModule(id string, export component.ExportFunc) (co
 		parent:                  m,
 	})
 
-	if err := m.o.ModuleRegistry.Register(fullPath, mod); err != nil {
-		return nil, err
-	}
-
-	m.modules[fullPath] = struct{}{}
 	return mod, nil
 }
 
-func (m *moduleController) removeID(id string) {
+func (m *moduleController) removeModule(mod *module) {
 	m.mut.Lock()
 	defer m.mut.Unlock()
 
-	delete(m.modules, id)
-	m.o.ModuleRegistry.Unregister(id)
+	m.o.ModuleRegistry.Unregister(mod.o.ID)
+	delete(m.modules, mod.o.ID)
+}
+
+func (m *moduleController) addModule(mod *module) error {
+	m.mut.Lock()
+	defer m.mut.Unlock()
+	if err := m.o.ModuleRegistry.Register(mod.o.ID, mod); err != nil {
+		level.Error(m.o.Logger).Log("msg", "error registering module", "id", mod.o.ID, "err", err)
+		return err
+	}
+	m.modules[mod.o.ID] = struct{}{}
+	return nil
 }
 
 // ModuleIDs implements [controller.ModuleController].
 func (m *moduleController) ModuleIDs() []string {
 	m.mut.RLock()
 	defer m.mut.RUnlock()
+
 	return maps.Keys(m.modules)
 }
 
@@ -86,7 +91,7 @@ type module struct {
 }
 
 type moduleOptions struct {
-	ID     string
+	ID     string // ID is the full name including all parents, "module.file.example.prometheus.remote_write.id".
 	export component.ExportFunc
 	parent *moduleController
 	*moduleControllerOptions
@@ -135,9 +140,14 @@ func (c *module) LoadConfig(config []byte, args map[string]any) error {
 // will be run until Run is called.
 //
 // Run blocks until the provided context is canceled.
-func (c *module) Run(ctx context.Context) {
-	defer c.o.parent.removeID(c.o.ID)
+func (c *module) Run(ctx context.Context) error {
+	if err := c.o.parent.addModule(c); err != nil {
+		return err
+	}
+	defer c.o.parent.removeModule(c)
+
 	c.f.Run(ctx)
+	return nil
 }
 
 // moduleControllerOptions holds static options for module controller.
diff --git a/pkg/flow/module_fail_test.go b/pkg/flow/module_fail_test.go
new file mode 100644
index 000000000000..28fb0923a892
--- /dev/null
+++ b/pkg/flow/module_fail_test.go
@@ -0,0 +1,76 @@
+package flow
+
+import (
+	"context"
+	"testing"
+	"time"
+
+	"github.com/grafana/agent/pkg/flow/componenttest"
+	"github.com/stretchr/testify/require"
+)
+
+func TestIDRemovalIfFailedToLoad(t *testing.T) {
+	f := New(testOptions(t))
+
+	fullContent := "test.fail.module \"t1\" { content = \"\" }"
+	fl, err := ParseSource("test", []byte(fullContent))
+	require.NoError(t, err)
+	err = f.LoadSource(fl, nil)
+	require.NoError(t, err)
+	ctx := context.Background()
+	ctx, cnc := context.WithTimeout(ctx, 600*time.Second)
+
+	go f.Run(ctx)
+	var t1 *componenttest.TestFailModule
+	require.Eventually(t, func() bool {
+		t1 = f.loader.Components()[0].Component().(*componenttest.TestFailModule)
+		return t1 != nil
+	}, 10*time.Second, 100*time.Millisecond)
+	require.Eventually(t, func() bool {
+		f.loadMut.RLock()
+		defer f.loadMut.RUnlock()
+		// This should be one due to t1.
+		return len(f.modules.List()) == 1
+	}, 10*time.Second, 100*time.Millisecond)
+	badContent :=
+		`test.fail.module "bad" {
+content=""
+fail=true
+}`
+	err = t1.UpdateContent(badContent)
+	// Because we have bad content this should fail, but the ids should be removed.
+	require.Error(t, err)
+	require.Eventually(t, func() bool {
+		f.loadMut.RLock()
+		defer f.loadMut.RUnlock()
+		// Only one since the bad one never should have been added.
+		rightLength := len(f.modules.List()) == 1
+		_, foundT1 := f.modules.Get("test.fail.module.t1")
+		return rightLength && foundT1
+	}, 10*time.Second, 100*time.Millisecond)
+	// fail a second time to ensure the once is done again.
+	err = t1.UpdateContent(badContent)
+	require.Error(t, err)
+
+	goodContent :=
+		`test.fail.module "good" { 
+content=""
+fail=false
+}`
+	err = t1.UpdateContent(goodContent)
+	require.NoError(t, err)
+	require.Eventually(t, func() bool {
+		f.loadMut.RLock()
+		defer f.loadMut.RUnlock()
+		modT1, foundT1 := f.modules.Get("test.fail.module.t1")
+		modGood, foundGood := f.modules.Get("test.fail.module.t1/test.fail.module.good")
+		return modT1 != nil && modGood != nil && foundT1 && foundGood
+	}, 10*time.Second, 100*time.Millisecond)
+	cnc()
+	require.Eventually(t, func() bool {
+		f.loadMut.RLock()
+		defer f.loadMut.RUnlock()
+		// All should be cleaned up.
+		return len(f.modules.List()) == 0
+	}, 10*time.Second, 100*time.Millisecond)
+}
diff --git a/pkg/flow/module_registry.go b/pkg/flow/module_registry.go
index 7b88dcaf717b..34e89fb6f4de 100644
--- a/pkg/flow/module_registry.go
+++ b/pkg/flow/module_registry.go
@@ -16,7 +16,7 @@ func newModuleRegistry() *moduleRegistry {
 	}
 }
 
-// Get retrives a module by ID.
+// Get retrieves a module by ID.
 func (reg *moduleRegistry) Get(id string) (*module, bool) {
 	reg.mut.RLock()
 	defer reg.mut.RUnlock()
diff --git a/pkg/flow/module_test.go b/pkg/flow/module_test.go
index d877bc4ba51c..0a371bc99a63 100644
--- a/pkg/flow/module_test.go
+++ b/pkg/flow/module_test.go
@@ -185,44 +185,58 @@ func TestIDList(t *testing.T) {
 	nc := newModuleController(o)
 	require.Len(t, nc.ModuleIDs(), 0)
 
-	_, err := nc.NewModule("t1", nil)
+	mod1, err := nc.NewModule("t1", nil)
 	require.NoError(t, err)
-	require.Len(t, nc.ModuleIDs(), 1)
-
-	_, err = nc.NewModule("t2", nil)
+	ctx := context.Background()
+	ctx, cncl := context.WithCancel(ctx)
+	go func() {
+		m1err := mod1.Run(ctx)
+		require.NoError(t, m1err)
+	}()
+	require.Eventually(t, func() bool {
+		return len(nc.ModuleIDs()) == 1
+	}, 1*time.Second, 100*time.Millisecond)
+
+	mod2, err := nc.NewModule("t2", nil)
 	require.NoError(t, err)
-	require.Len(t, nc.ModuleIDs(), 2)
+	go func() {
+		m2err := mod2.Run(ctx)
+		require.NoError(t, m2err)
+	}()
+	require.Eventually(t, func() bool {
+		return len(nc.ModuleIDs()) == 2
+	}, 1*time.Second, 100*time.Millisecond)
+	// Call cncl which will stop the run methods and remove the ids from the module controller
+	cncl()
+	require.Eventually(t, func() bool {
+		return len(nc.ModuleIDs()) == 0
+	}, 1*time.Second, 100*time.Millisecond)
 }
 
-func TestIDCollision(t *testing.T) {
+func TestDuplicateIDList(t *testing.T) {
 	defer verifyNoGoroutineLeaks(t)
 	o := testModuleControllerOptions(t)
 	defer o.WorkerPool.Stop()
 	nc := newModuleController(o)
-	m, err := nc.NewModule("t1", nil)
-	require.NoError(t, err)
-	require.NotNil(t, m)
-	m, err = nc.NewModule("t1", nil)
-	require.Error(t, err)
-	require.Nil(t, m)
-}
+	require.Len(t, nc.ModuleIDs(), 0)
 
-func TestIDRemoval(t *testing.T) {
-	defer verifyNoGoroutineLeaks(t)
-	opts := testModuleControllerOptions(t)
-	defer opts.WorkerPool.Stop()
-	opts.ID = "test"
-	nc := newModuleController(opts)
-	m, err := nc.NewModule("t1", func(exports map[string]any) {})
-	require.NoError(t, err)
-	err = m.LoadConfig([]byte(""), nil)
+	mod1, err := nc.NewModule("t1", nil)
 	require.NoError(t, err)
-	require.NotNil(t, m)
 	ctx := context.Background()
-	ctx, cncl := context.WithTimeout(ctx, 1*time.Second)
+	ctx, cncl := context.WithCancel(ctx)
 	defer cncl()
-	m.Run(ctx)
-	require.Len(t, nc.(*moduleController).modules, 0)
+	go func() {
+		m1err := mod1.Run(ctx)
+		require.NoError(t, m1err)
+	}()
+	require.Eventually(t, func() bool {
+		return len(nc.ModuleIDs()) == 1
+	}, 5*time.Second, 100*time.Millisecond)
+
+	// This should panic with duplicate registration.
+	require.PanicsWithError(t, "duplicate metrics collector registration attempted", func() {
+		_, _ = nc.NewModule("t1", nil)
+	})
 }
 
 func testModuleControllerOptions(t *testing.T) *moduleControllerOptions {