diff --git a/.chloggen/supervisor_restart_command_capability.yaml b/.chloggen/supervisor_restart_command_capability.yaml
new file mode 100644
index 000000000000..e984ef510354
--- /dev/null
+++ b/.chloggen/supervisor_restart_command_capability.yaml
@@ -0,0 +1,27 @@
+# Use this changelog template to create an entry for release notes.
+
+# One of 'breaking', 'deprecation', 'new_component', 'enhancement', 'bug_fix'
+change_type: enhancement
+
+# The name of the component, or a single word describing the area of concern, (e.g. filelogreceiver)
+component: cmd/opampsupervisor
+
+# A brief description of the change.  Surround your text with quotes ("") if it needs to start with a backtick (`).
+note: Support AcceptsRestartCommand Capability.
+
+# Mandatory: One or more tracking issues related to the change. You can use the PR number here if no issue exists.
+issues: [21077]
+
+# (Optional) One or more lines of additional information to render under the primary note.
+# These lines will be padded with 2 spaces and then inserted directly into the document.
+# Use pipe (|) for multiline entries.
+subtext:
+
+# If your change doesn't affect end users or the exported elements of any package,
+# you should instead start your pull request title with [chore] or use the "Skip Changelog" label.
+# Optional: The change log or logs in which this entry should be included.
+# e.g. '[user]' or '[user, api]'
+# Include 'user' if the change is relevant to end users.
+# Include 'api' if there is a change to a library API.
+# Default: '[user]'
+change_logs: []
diff --git a/cmd/opampsupervisor/e2e_test.go b/cmd/opampsupervisor/e2e_test.go
index 274bcc1d4678..0be9c6cfe532 100644
--- a/cmd/opampsupervisor/e2e_test.go
+++ b/cmd/opampsupervisor/e2e_test.go
@@ -474,6 +474,87 @@ func waitForSupervisorConnection(connection chan bool, connected bool) {
 	}
 }
 
+func TestSupervisorRestartCommand(t *testing.T) {
+	var healthReport atomic.Value
+	var agentConfig atomic.Value
+	server := newOpAMPServer(
+		t,
+		defaultConnectingHandler,
+		server.ConnectionCallbacksStruct{
+			OnMessageFunc: func(_ context.Context, _ types.Connection, message *protobufs.AgentToServer) *protobufs.ServerToAgent {
+				if message.Health != nil {
+					healthReport.Store(message.Health)
+				}
+
+				if message.EffectiveConfig != nil {
+					config := message.EffectiveConfig.ConfigMap.ConfigMap[""]
+					if config != nil {
+						agentConfig.Store(string(config.Body))
+					}
+				}
+				return &protobufs.ServerToAgent{}
+			},
+		})
+
+	s := newSupervisor(t, "basic", map[string]string{"url": server.addr})
+	defer s.Shutdown()
+
+	waitForSupervisorConnection(server.supervisorConnected, true)
+
+	// Send the initial config
+	cfg, hash, _, _ := createSimplePipelineCollectorConf(t)
+
+	server.sendToSupervisor(&protobufs.ServerToAgent{
+		RemoteConfig: &protobufs.AgentRemoteConfig{
+			Config: &protobufs.AgentConfigMap{
+				ConfigMap: map[string]*protobufs.AgentConfigFile{
+					"": {Body: cfg.Bytes()},
+				},
+			},
+			ConfigHash: hash,
+		},
+	})
+
+	require.Eventually(t, func() bool {
+		cfg, ok := agentConfig.Load().(string)
+		if ok {
+			return strings.Contains(cfg, "health_check")
+		}
+		return false
+	}, 5*time.Second, 500*time.Millisecond, "Collector was not started with healthcheck")
+
+	require.Eventually(t, func() bool {
+		health := healthReport.Load().(*protobufs.ComponentHealth)
+
+		if health != nil {
+			return health.Healthy && health.LastError == ""
+		}
+
+		return false
+	}, 5*time.Second, 500*time.Millisecond, "Collector never became healthy")
+
+	// The health report should be received after the restart
+	healthReport.Store(&protobufs.ComponentHealth{})
+
+	server.sendToSupervisor(&protobufs.ServerToAgent{
+		Command: &protobufs.ServerToAgentCommand{
+			Type: protobufs.CommandType_CommandType_Restart,
+		},
+	})
+
+	server.sendToSupervisor(&protobufs.ServerToAgent{
+		Flags: uint64(protobufs.ServerToAgentFlags_ServerToAgentFlags_ReportFullState),
+	})
+
+	require.Eventually(t, func() bool {
+		health := healthReport.Load().(*protobufs.ComponentHealth)
+		if health != nil {
+			return health.Healthy && health.LastError == ""
+		}
+		return false
+	}, 10*time.Second, 250*time.Millisecond, "Collector never reported healthy after restart")
+}
+
 func TestSupervisorOpAMPConnectionSettings(t *testing.T) {
 	var connectedToNewServer atomic.Bool
 	initialServer := newOpAMPServer(
diff --git a/cmd/opampsupervisor/supervisor/commander/commander.go b/cmd/opampsupervisor/supervisor/commander/commander.go
index 7457f23693da..3445058ee862 100644
--- a/cmd/opampsupervisor/supervisor/commander/commander.go
+++ b/cmd/opampsupervisor/supervisor/commander/commander.go
@@ -99,6 +99,7 @@ func (c *Commander) Start(ctx context.Context) error {
 }
 
 func (c *Commander) Restart(ctx context.Context) error {
+	c.logger.Debug("Restarting agent", zap.String("agent", c.cfg.Executable))
 	if err := c.Stop(ctx); err != nil {
 		return err
 	}
diff --git a/cmd/opampsupervisor/supervisor/config/config.go b/cmd/opampsupervisor/supervisor/config/config.go
index 1948b42a0701..ff020f00db0c 100644
--- a/cmd/opampsupervisor/supervisor/config/config.go
+++ b/cmd/opampsupervisor/supervisor/config/config.go
@@ -19,6 +19,7 @@ type Supervisor struct {
 // Capabilities is the set of capabilities that the Supervisor supports.
 type Capabilities struct {
 	AcceptsRemoteConfig            *bool `mapstructure:"accepts_remote_config"`
+	AcceptsRestartCommand          *bool `mapstructure:"accepts_restart_command"`
 	AcceptsOpAMPConnectionSettings *bool `mapstructure:"accepts_opamp_connection_settings"`
 	ReportsEffectiveConfig         *bool `mapstructure:"reports_effective_config"`
 	ReportsOwnMetrics              *bool `mapstructure:"reports_own_metrics"`
diff --git a/cmd/opampsupervisor/supervisor/supervisor.go b/cmd/opampsupervisor/supervisor/supervisor.go
index d7e91aedfba9..1aa757a54290 100644
--- a/cmd/opampsupervisor/supervisor/supervisor.go
+++ b/cmd/opampsupervisor/supervisor/supervisor.go
@@ -107,6 +107,7 @@ type Supervisor struct {
 
 	agentHasStarted               bool
 	agentStartHealthCheckAttempts int
+	agentRestarting               atomic.Bool
 
 	connectedToOpAMPServer chan struct{}
 }
@@ -345,6 +346,10 @@ func (s *Supervisor) Capabilities() protobufs.AgentCapabilities {
 			supportedCapabilities |= protobufs.AgentCapabilities_AgentCapabilities_ReportsRemoteConfig
 		}
 
+		if c.AcceptsRestartCommand != nil && *c.AcceptsRestartCommand {
+			supportedCapabilities |= protobufs.AgentCapabilities_AgentCapabilities_AcceptsRestartCommand
+		}
+
 		if c.AcceptsOpAMPConnectionSettings != nil && *c.AcceptsOpAMPConnectionSettings {
 			supportedCapabilities |= protobufs.AgentCapabilities_AgentCapabilities_AcceptsOpAMPConnectionSettings
 		}
@@ -386,8 +391,7 @@ func (s *Supervisor) startOpAMP() error {
 			OnCommandFunc: func(_ context.Context, command *protobufs.ServerToAgentCommand) error {
 				cmdType := command.GetType()
 				if *cmdType.Enum() == protobufs.CommandType_CommandType_Restart {
-					// TODO: https://github.com/open-telemetry/opentelemetry-collector-contrib/issues/21077
-					s.logger.Debug("Received restart command")
+					return s.handleRestartCommand()
 				}
 				return nil
 			},
@@ -699,6 +703,17 @@ func (s *Supervisor) recalcEffectiveConfig() (configChanged bool, err error) {
 	return configChanged, nil
 }
 
+func (s *Supervisor) handleRestartCommand() error {
+	s.agentRestarting.Store(true)
+	defer s.agentRestarting.Store(false)
+	s.logger.Debug("Received restart command")
+	err := s.commander.Restart(context.Background())
+	if err != nil {
+		s.logger.Error("Could not restart agent process", zap.Error(err))
+	}
+	return err
+}
+
 func (s *Supervisor) startAgent() {
 	err := s.commander.Start(context.Background())
 	if err != nil {
@@ -792,6 +807,11 @@ func (s *Supervisor) runAgentProcess() {
 			s.startAgent()
 
 		case <-s.commander.Exited():
+			// the agent process exit is expected for restart command and will not attempt to restart
+			if s.agentRestarting.Load() {
+				continue
+			}
+
 			if s.shuttingDown {
 				return
 			}
diff --git a/cmd/opampsupervisor/testdata/supervisor/supervisor_basic.yaml b/cmd/opampsupervisor/testdata/supervisor/supervisor_basic.yaml
index b5ef4c5db720..7e4b0a08536c 100644
--- a/cmd/opampsupervisor/testdata/supervisor/supervisor_basic.yaml
+++ b/cmd/opampsupervisor/testdata/supervisor/supervisor_basic.yaml
@@ -9,6 +9,7 @@ capabilities:
   reports_health: true
   accepts_remote_config: true
   reports_remote_config: true
+  accepts_restart_command: true
 
 agent:
   executable: ../../bin/otelcontribcol_{{.goos}}_{{.goarch}}{{.extension}}