diff --git a/services/server/config/config.go b/services/server/config/config.go
index 0f395f040..4d57f6cfa 100644
--- a/services/server/config/config.go
+++ b/services/server/config/config.go
@@ -43,6 +43,13 @@ import (
 // CurrentConfigVersion is the max config version which is supported
 const CurrentConfigVersion = 3
 
+// migrations hold the migration functions for every prior containerd config version
+var migrations = []func(context.Context, *Config) error{
+	nil,       // Version 0 is not defined, treated at version 1
+	v1Migrate, // Version 1 plugins renamed to URI for version 2
+	nil,       // Version 2 has only plugin changes to version 3
+}
+
 // NOTE: Any new map fields added also need to be handled in mergeConfig.
 
 // Config provides containerd configuration data for the server
@@ -67,9 +74,11 @@ type Config struct {
 	Metrics MetricsConfig `toml:"metrics"`
 	// DisabledPlugins are IDs of plugins to disable. Disabled plugins won't be
 	// initialized and started.
+	// DisabledPlugins must use a fully qualified plugin URI.
 	DisabledPlugins []string `toml:"disabled_plugins"`
 	// RequiredPlugins are IDs of required plugins. Containerd exits if any
 	// required plugin doesn't exist or fails to be initialized or started.
+	// RequiredPlugins must use a fully qualified plugin URI.
 	RequiredPlugins []string `toml:"required_plugins"`
 	// Plugins provides plugin specific configuration for the initialization of a plugin
 	Plugins map[string]interface{} `toml:"plugins"`
@@ -101,44 +110,86 @@ type StreamProcessor struct {
 	Env []string `toml:"env"`
 }
 
-// GetVersion returns the config file's version
-func (c *Config) GetVersion() int {
-	if c.Version == 0 {
-		return 1
-	}
-	return c.Version
-}
-
 // ValidateVersion validates the config for a v2 file
 func (c *Config) ValidateVersion() error {
-	version := c.GetVersion()
-	if version == 1 {
-		return errors.New("containerd config version `1` is no longer supported since containerd v2.0, please switch to version `2`, " +
-			"see https://github.com/containerd/containerd/blob/main/docs/PLUGINS.md#version-header")
-	}
-
-	if version > CurrentConfigVersion {
-		return fmt.Errorf("expected containerd config version equal to or less than `%d`, got `%d`", CurrentConfigVersion, version)
+	if c.Version > CurrentConfigVersion {
+		return fmt.Errorf("expected containerd config version equal to or less than `%d`, got `%d`", CurrentConfigVersion, c.Version)
 	}
 
 	for _, p := range c.DisabledPlugins {
-		if !strings.HasPrefix(p, "io.containerd.") || len(strings.SplitN(p, ".", 4)) < 4 {
+		if !strings.ContainsAny(p, ".") {
 			return fmt.Errorf("invalid disabled plugin URI %q expect io.containerd.x.vx", p)
 		}
 	}
 	for _, p := range c.RequiredPlugins {
-		if !strings.HasPrefix(p, "io.containerd.") || len(strings.SplitN(p, ".", 4)) < 4 {
+		if !strings.ContainsAny(p, ".") {
 			return fmt.Errorf("invalid required plugin URI %q expect io.containerd.x.vx", p)
 		}
 	}
-	for p := range c.Plugins {
-		if !strings.HasPrefix(p, "io.containerd.") || len(strings.SplitN(p, ".", 4)) < 4 {
-			return fmt.Errorf("invalid plugin key URI %q expect io.containerd.x.vx", p)
+
+	return nil
+}
+
+// MigrateConfig will convert the config to the latest version before using
+func (c *Config) MigrateConfig(ctx context.Context) error {
+	for c.Version < CurrentConfigVersion {
+		if m := migrations[c.Version]; m != nil {
+			if err := m(ctx, c); err != nil {
+				return err
+			}
 		}
+		c.Version++
 	}
 	return nil
 }
 
+func v1Migrate(ctx context.Context, c *Config) error {
+	plugins := make(map[string]interface{}, len(c.Plugins))
+
+	// corePlugins is the list of used plugins before v1 was deprecated
+	corePlugins := map[string]string{
+		"cri":       "io.containerd.grpc.v1.cri",
+		"cgroups":   "io.containerd.monitor.v1.cgroups",
+		"linux":     "io.containerd.runtime.v1.linux",
+		"scheduler": "io.containerd.gc.v1.scheduler",
+		"bolt":      "io.containerd.metadata.v1.bolt",
+		"task":      "io.containerd.runtime.v2.task",
+		"opt":       "io.containerd.internal.v1.opt",
+		"restart":   "io.containerd.internal.v1.restart",
+		"tracing":   "io.containerd.internal.v1.tracing",
+		"otlp":      "io.containerd.tracing.processor.v1.otlp",
+		"aufs":      "io.containerd.snapshotter.v1.aufs",
+		"btrfs":     "io.containerd.snapshotter.v1.btrfs",
+		"devmapper": "io.containerd.snapshotter.v1.devmapper",
+		"native":    "io.containerd.snapshotter.v1.native",
+		"overlayfs": "io.containerd.snapshotter.v1.overlayfs",
+		"zfs":       "io.containerd.snapshotter.v1.zfs",
+	}
+	for plugin, value := range c.Plugins {
+		if !strings.ContainsAny(plugin, ".") {
+			var ambiguous string
+			if full, ok := corePlugins[plugin]; ok {
+				plugin = full
+			} else if strings.HasSuffix(plugin, "-service") {
+				plugin = "io.containerd.service.v1." + plugin
+			} else if plugin == "windows" || plugin == "windows-lcow" {
+				// runtime, differ, and snapshotter plugins do not have configs for v1
+				ambiguous = plugin
+				plugin = "io.containerd.snapshotter.v1." + plugin
+			} else {
+				ambiguous = plugin
+				plugin = "io.containerd.grpc.v1." + plugin
+			}
+			if ambiguous != "" {
+				log.G(ctx).Warnf("Ambiguous %s plugin in v1 config, treating as %s", ambiguous, plugin)
+			}
+		}
+		plugins[plugin] = value
+	}
+	c.Plugins = plugins
+	return nil
+}
+
 // GRPCConfig provides GRPC configuration for the socket
 type GRPCConfig struct {
 	Address        string `toml:"address"`
diff --git a/services/server/config/config_test.go b/services/server/config/config_test.go
index 9932f1ecb..742af453f 100644
--- a/services/server/config/config_test.go
+++ b/services/server/config/config_test.go
@@ -29,6 +29,12 @@ import (
 	"github.com/containerd/log/logtest"
 )
 
+func TestMigrations(t *testing.T) {
+	if len(migrations) != CurrentConfigVersion {
+		t.Fatalf("Migration missing, expected %d migrations, only %d defined", CurrentConfigVersion, len(migrations))
+	}
+}
+
 func TestMergeConfigs(t *testing.T) {
 	a := &Config{
 		Version:          2,
@@ -215,9 +221,10 @@ version = 2
 	assert.Equal(t, true, pluginConfig["shim_debug"])
 }
 
-// TestDecodePluginInV1Config tests decoding non-versioned
-// config (should be parsed as V1 config).
+// TestDecodePluginInV1Config tests decoding non-versioned config
+// (should be parsed as V1 config) and migrated to latest.
 func TestDecodePluginInV1Config(t *testing.T) {
+	ctx := logtest.WithT(context.Background(), t)
 	data := `
 [plugins.linux]
   shim_debug = true
@@ -229,5 +236,15 @@ func TestDecodePluginInV1Config(t *testing.T) {
 
 	var out Config
 	err = LoadConfig(context.Background(), path, &out)
-	assert.ErrorContains(t, err, "config version `1` is no longer supported")
+	assert.NoError(t, err)
+	assert.Equal(t, 0, out.Version)
+
+	err = out.MigrateConfig(ctx)
+	assert.NoError(t, err)
+	assert.Equal(t, 3, out.Version)
+
+	pluginConfig := map[string]interface{}{}
+	_, err = out.Decode(ctx, &plugin.Registration{Type: "io.containerd.runtime.v1", ID: "linux", Config: &pluginConfig})
+	assert.NoError(t, err)
+	assert.Equal(t, true, pluginConfig["shim_debug"])
 }
diff --git a/services/server/server.go b/services/server/server.go
index e1c5d7384..95310b0cd 100644
--- a/services/server/server.go
+++ b/services/server/server.go
@@ -103,6 +103,20 @@ func CreateTopLevelDirectories(config *srvconfig.Config) error {
 
 // New creates and initializes a new containerd server
 func New(ctx context.Context, config *srvconfig.Config) (*Server, error) {
+	var (
+		version    = config.Version
+		migrationT time.Duration
+	)
+	if version < srvconfig.CurrentConfigVersion {
+		// Migrate config to latest version
+		t1 := time.Now()
+		err := config.MigrateConfig(ctx)
+		if err != nil {
+			return nil, err
+		}
+		migrationT = time.Since(t1)
+	}
+
 	if err := apply(ctx, config); err != nil {
 		return nil, err
 	}
@@ -203,17 +217,24 @@ func New(ctx context.Context, config *srvconfig.Config) (*Server, error) {
 		required[r] = struct{}{}
 	}
 
-	// Run migration for each configuration version
-	// Run each plugin migration for each version to ensure that migration logic is simple and
-	// focused on upgrading from one version at a time.
-	for v := config.Version; v < srvconfig.CurrentConfigVersion; v++ {
-		for _, p := range plugins {
-			if p.ConfigMigration != nil {
-				if err := p.ConfigMigration(ctx, v, config.Plugins); err != nil {
-					return nil, err
+	if version < srvconfig.CurrentConfigVersion {
+		t1 := time.Now()
+		// Run migration for each configuration version
+		// Run each plugin migration for each version to ensure that migration logic is simple and
+		// focused on upgrading from one version at a time.
+		for v := version; v < srvconfig.CurrentConfigVersion; v++ {
+			for _, p := range plugins {
+				if p.ConfigMigration != nil {
+					if err := p.ConfigMigration(ctx, v, config.Plugins); err != nil {
+						return nil, err
+					}
 				}
 			}
 		}
+		migrationT = migrationT + time.Since(t1)
+	}
+	if migrationT > 0 {
+		log.G(ctx).WithField("t", migrationT).Warnf("Configuration migrated from version %d, use `containerd config migrate` to avoid migration", version)
 	}
 
 	for _, p := range plugins {