diff --git a/.chloggen/fix-onmessage.yaml b/.chloggen/fix-onmessage.yaml
new file mode 100644
index 000000000000..8ed7500ed069
--- /dev/null
+++ b/.chloggen/fix-onmessage.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: bug_fix
+
+# 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: Ensure the Supervisor processes all fields in a ServerToAgent message.
+
+# Mandatory: One or more tracking issues related to the change. You can use the PR number here if no issue exists.
+issues: [34349]
+
+# (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/supervisor/supervisor.go b/cmd/opampsupervisor/supervisor/supervisor.go
index 3ef418a68f14..e20fb7808526 100644
--- a/cmd/opampsupervisor/supervisor/supervisor.go
+++ b/cmd/opampsupervisor/supervisor/supervisor.go
@@ -1180,16 +1180,17 @@ func (s *Supervisor) saveLastReceivedOwnTelemetrySettings(set *protobufs.Telemet
 
 func (s *Supervisor) onMessage(ctx context.Context, msg *types.MessageData) {
 	configChanged := false
-	if msg.RemoteConfig != nil {
-		configChanged = configChanged || s.processRemoteConfigMessage(msg.RemoteConfig)
+
+	if msg.AgentIdentification != nil {
+		configChanged = s.processAgentIdentificationMessage(msg.AgentIdentification) || configChanged
 	}
 
-	if msg.OwnMetricsConnSettings != nil {
-		configChanged = configChanged || s.processOwnMetricsConnSettingsMessage(ctx, msg.OwnMetricsConnSettings)
+	if msg.RemoteConfig != nil {
+		configChanged = s.processRemoteConfigMessage(msg.RemoteConfig) || configChanged
 	}
 
-	if msg.AgentIdentification != nil {
-		configChanged = configChanged || s.processAgentIdentificationMessage(msg.AgentIdentification)
+	if msg.OwnMetricsConnSettings != nil {
+		configChanged = s.processOwnMetricsConnSettingsMessage(ctx, msg.OwnMetricsConnSettings) || configChanged
 	}
 
 	// Update the agent config if any messages have touched the config
@@ -1299,7 +1300,14 @@ func (s *Supervisor) processAgentIdentificationMessage(msg *protobufs.AgentIdent
 		s.logger.Error("Failed to send agent description to OpAMP server")
 	}
 
-	return true
+	// Need to recalculate the Agent config so that the new agent identification is included in it.
+	configChanged, err := s.composeMergedConfig(s.remoteConfig)
+	if err != nil {
+		s.logger.Error("Error composing merged config with new instance ID", zap.Error(err))
+		return false
+	}
+
+	return configChanged
 }
 
 func (s *Supervisor) persistentStateFile() string {
diff --git a/cmd/opampsupervisor/supervisor/supervisor_test.go b/cmd/opampsupervisor/supervisor/supervisor_test.go
index 1af3653e05cc..3fdd1372b175 100644
--- a/cmd/opampsupervisor/supervisor/supervisor_test.go
+++ b/cmd/opampsupervisor/supervisor/supervisor_test.go
@@ -104,10 +104,12 @@ func Test_onMessage(t *testing.T) {
 			persistentState:              &persistentState{InstanceID: initialID},
 			agentDescription:             agentDesc,
 			agentConfigOwnMetricsSection: &atomic.Value{},
+			mergedConfig:                 &atomic.Value{},
 			effectiveConfig:              &atomic.Value{},
 			agentHealthCheckEndpoint:     "localhost:8000",
 			opampClient:                  client.NewHTTP(newLoggerFromZap(zap.NewNop())),
 		}
+		require.NoError(t, s.createTemplates())
 
 		s.onMessage(context.Background(), &types.MessageData{
 			AgentIdentification: &protobufs.AgentIdentification{
@@ -131,9 +133,11 @@ func Test_onMessage(t *testing.T) {
 			persistentState:              &persistentState{InstanceID: testUUID},
 			agentDescription:             agentDesc,
 			agentConfigOwnMetricsSection: &atomic.Value{},
+			mergedConfig:                 &atomic.Value{},
 			effectiveConfig:              &atomic.Value{},
 			agentHealthCheckEndpoint:     "localhost:8000",
 		}
+		require.NoError(t, s.createTemplates())
 
 		s.onMessage(context.Background(), &types.MessageData{
 			AgentIdentification: &protobufs.AgentIdentification{
@@ -175,6 +179,7 @@ func Test_onMessage(t *testing.T) {
 			hasNewConfig:                 make(chan struct{}, 1),
 			persistentState:              &persistentState{InstanceID: testUUID},
 			agentConfigOwnMetricsSection: &atomic.Value{},
+			mergedConfig:                 &atomic.Value{},
 			effectiveConfig:              &atomic.Value{},
 			agentConn:                    agentConnAtomic,
 			agentHealthCheckEndpoint:     "localhost:8000",
@@ -231,6 +236,61 @@ func Test_onMessage(t *testing.T) {
 		require.True(t, gotMessage, "Message was not sent to agent")
 	})
 
+	t.Run("Processes all ServerToAgent fields", func(t *testing.T) {
+		agentDesc := &atomic.Value{}
+		agentDesc.Store(&protobufs.AgentDescription{
+			NonIdentifyingAttributes: []*protobufs.KeyValue{
+				{
+					Key: "runtime.type",
+					Value: &protobufs.AnyValue{
+						Value: &protobufs.AnyValue_StringValue{
+							StringValue: "test",
+						},
+					},
+				},
+			},
+		})
+		initialID := uuid.MustParse("018fee23-4a51-7303-a441-73faed7d9deb")
+		newID := uuid.MustParse("018fef3f-14a8-73ef-b63e-3b96b146ea38")
+		s := Supervisor{
+			logger:                       zap.NewNop(),
+			pidProvider:                  defaultPIDProvider{},
+			config:                       config.Supervisor{},
+			hasNewConfig:                 make(chan struct{}, 1),
+			persistentState:              &persistentState{InstanceID: initialID},
+			agentDescription:             agentDesc,
+			agentConfigOwnMetricsSection: &atomic.Value{},
+			mergedConfig:                 &atomic.Value{},
+			effectiveConfig:              &atomic.Value{},
+			agentHealthCheckEndpoint:     "localhost:8000",
+			opampClient:                  client.NewHTTP(newLoggerFromZap(zap.NewNop())),
+		}
+		require.NoError(t, s.createTemplates())
+
+		s.onMessage(context.Background(), &types.MessageData{
+			AgentIdentification: &protobufs.AgentIdentification{
+				NewInstanceUid: newID[:],
+			},
+			RemoteConfig: &protobufs.AgentRemoteConfig{
+				Config: &protobufs.AgentConfigMap{
+					ConfigMap: map[string]*protobufs.AgentConfigFile{
+						"": {
+							Body: []byte(""),
+						},
+					},
+				},
+			},
+			OwnMetricsConnSettings: &protobufs.TelemetryConnectionSettings{
+				DestinationEndpoint: "http://localhost:4318",
+			},
+		})
+
+		require.Equal(t, newID, s.persistentState.InstanceID)
+		t.Log(s.mergedConfig.Load())
+		require.Contains(t, s.mergedConfig.Load(), "prometheus/own_metrics")
+		require.Contains(t, s.mergedConfig.Load(), newID.String())
+		require.Contains(t, s.mergedConfig.Load(), "runtime.type: test")
+	})
 }
 
 func Test_handleAgentOpAMPMessage(t *testing.T) {