diff --git a/pkg/agent/context.go b/pkg/agent/context.go
index 5a84c45e2..eba516c39 100644
--- a/pkg/agent/context.go
+++ b/pkg/agent/context.go
@@ -222,13 +222,10 @@ func (cb *ContextBuilder) InvalidateCache() {
 // invalidation (bootstrap files + memory). Skill roots are handled separately
 // because they require both directory-level and recursive file-level checks.
 func (cb *ContextBuilder) sourcePaths() []string {
-	return []string{
-		filepath.Join(cb.workspace, "AGENTS.md"),
-		filepath.Join(cb.workspace, "SOUL.md"),
-		filepath.Join(cb.workspace, "USER.md"),
-		filepath.Join(cb.workspace, "IDENTITY.md"),
-		filepath.Join(cb.workspace, "memory", "MEMORY.md"),
-	}
+	agentDefinition := cb.LoadAgentDefinition()
+	paths := agentDefinition.trackedPaths(cb.workspace)
+	paths = append(paths, filepath.Join(cb.workspace, "memory", "MEMORY.md"))
+	return uniquePaths(paths)
 }
 
 // skillRoots returns all skill root directories that can affect
@@ -432,18 +429,29 @@ func skillFilesChangedSince(skillRoots []string, filesAtCache map[string]time.Ti
 }
 
 func (cb *ContextBuilder) LoadBootstrapFiles() string {
-	bootstrapFiles := []string{
-		"AGENTS.md",
-		"SOUL.md",
-		"USER.md",
-		"IDENTITY.md",
+	var sb strings.Builder
+
+	agentDefinition := cb.LoadAgentDefinition()
+	if agentDefinition.Agent != nil {
+		label := string(agentDefinition.Source)
+		if label == "" {
+			label = relativeWorkspacePath(cb.workspace, agentDefinition.Agent.Path)
+		}
+		fmt.Fprintf(&sb, "## %s\n\n%s\n\n", label, agentDefinition.Agent.Body)
+	}
+	if agentDefinition.Soul != nil {
+		fmt.Fprintf(
+			&sb,
+			"## %s\n\n%s\n\n",
+			relativeWorkspacePath(cb.workspace, agentDefinition.Soul.Path),
+			agentDefinition.Soul.Content,
+		)
 	}
 
-	var sb strings.Builder
-	for _, filename := range bootstrapFiles {
-		filePath := filepath.Join(cb.workspace, filename)
+	if agentDefinition.Source != AgentDefinitionSourceAgent {
+		filePath := filepath.Join(cb.workspace, "IDENTITY.md")
 		if data, err := os.ReadFile(filePath); err == nil {
-			fmt.Fprintf(&sb, "## %s\n\n%s\n\n", filename, data)
+			fmt.Fprintf(&sb, "## %s\n\n%s\n\n", "IDENTITY.md", data)
 		}
 	}
 
diff --git a/pkg/agent/context_cache_test.go b/pkg/agent/context_cache_test.go
index 707510820..1f9423a3a 100644
--- a/pkg/agent/context_cache_test.go
+++ b/pkg/agent/context_cache_test.go
@@ -37,7 +37,7 @@ func setupWorkspace(t *testing.T, files map[string]string) string {
 // Codex (only reads last system message as instructions).
 func TestSingleSystemMessage(t *testing.T) {
 	tmpDir := setupWorkspace(t, map[string]string{
-		"IDENTITY.md": "# Identity\nTest agent.",
+		"AGENT.md": "# Agent\nTest agent.",
 	})
 	defer os.RemoveAll(tmpDir)
 
@@ -140,10 +140,10 @@ func TestMtimeAutoInvalidation(t *testing.T) {
 	}{
 		{
 			name:       "bootstrap file change",
-			file:       "IDENTITY.md",
-			contentV1:  "# Original Identity",
-			contentV2:  "# Updated Identity",
-			checkField: "Updated Identity",
+			file:       "AGENT.md",
+			contentV1:  "# Original Agent",
+			contentV2:  "# Updated Agent",
+			checkField: "Updated Agent",
 		},
 		{
 			name:       "memory file change",
@@ -218,7 +218,7 @@ func TestMtimeAutoInvalidation(t *testing.T) {
 // even when source files haven't changed (useful for tests and reload commands).
 func TestExplicitInvalidateCache(t *testing.T) {
 	tmpDir := setupWorkspace(t, map[string]string{
-		"IDENTITY.md": "# Test Identity",
+		"AGENT.md": "# Test Agent",
 	})
 	defer os.RemoveAll(tmpDir)
 
@@ -245,8 +245,8 @@ func TestExplicitInvalidateCache(t *testing.T) {
 // when no files change (regression test for issue #607).
 func TestCacheStability(t *testing.T) {
 	tmpDir := setupWorkspace(t, map[string]string{
-		"IDENTITY.md": "# Identity\nContent",
-		"SOUL.md":     "# Soul\nContent",
+		"AGENT.md": "# Agent\nContent",
+		"SOUL.md":  "# Soul\nContent",
 	})
 	defer os.RemoveAll(tmpDir)
 
@@ -545,7 +545,7 @@ description: delete-me-v1
 // Run with: go test -race ./pkg/agent/ -run TestConcurrentBuildSystemPromptWithCache
 func TestConcurrentBuildSystemPromptWithCache(t *testing.T) {
 	tmpDir := setupWorkspace(t, map[string]string{
-		"IDENTITY.md":          "# Identity\nConcurrency test agent.",
+		"AGENT.md":             "# Agent\nConcurrency test agent.",
 		"SOUL.md":              "# Soul\nBe helpful.",
 		"memory/MEMORY.md":     "# Memory\nUser prefers Go.",
 		"skills/demo/SKILL.md": "---\nname: demo\ndescription: \"demo skill\"\n---\n# Demo",
@@ -652,7 +652,7 @@ func BenchmarkBuildMessagesWithCache(b *testing.B) {
 
 	os.MkdirAll(filepath.Join(tmpDir, "memory"), 0o755)
 	os.MkdirAll(filepath.Join(tmpDir, "skills"), 0o755)
-	for _, name := range []string{"IDENTITY.md", "SOUL.md", "USER.md"} {
+	for _, name := range []string{"AGENT.md", "SOUL.md"} {
 		os.WriteFile(filepath.Join(tmpDir, name), []byte(strings.Repeat("Content.\n", 10)), 0o644)
 	}
 
diff --git a/pkg/agent/definition_test.go b/pkg/agent/definition_test.go
new file mode 100644
index 000000000..e643dc047
--- /dev/null
+++ b/pkg/agent/definition_test.go
@@ -0,0 +1,189 @@
+package agent
+
+import (
+	"os"
+	"path/filepath"
+	"strings"
+	"testing"
+	"time"
+)
+
+func TestLoadAgentDefinitionParsesFrontmatterAndSoul(t *testing.T) {
+	tmpDir := setupWorkspace(t, map[string]string{
+		"AGENT.md": `---
+name: pico
+description: Structured agent
+model: claude-3-7-sonnet
+tools:
+  - shell
+  - search
+maxTurns: 8
+skills:
+  - review
+  - search-docs
+mcpServers:
+  - github
+metadata:
+  mode: strict
+---
+# Agent
+
+Act directly and use tools first.
+`,
+		"SOUL.md": "# Soul\nStay precise.",
+	})
+	defer cleanupWorkspace(t, tmpDir)
+
+	cb := NewContextBuilder(tmpDir)
+	definition := cb.LoadAgentDefinition()
+
+	if definition.Source != AgentDefinitionSourceAgent {
+		t.Fatalf("expected source %q, got %q", AgentDefinitionSourceAgent, definition.Source)
+	}
+	if definition.Agent == nil {
+		t.Fatal("expected AGENT.md definition to be loaded")
+	}
+	if definition.Agent.Body == "" || !strings.Contains(definition.Agent.Body, "Act directly") {
+		t.Fatalf("expected AGENT.md body to be preserved, got %q", definition.Agent.Body)
+	}
+	if definition.Agent.Frontmatter.Name != "pico" {
+		t.Fatalf("expected name to be parsed, got %q", definition.Agent.Frontmatter.Name)
+	}
+	if definition.Agent.Frontmatter.Model != "claude-3-7-sonnet" {
+		t.Fatalf("expected model to be parsed, got %q", definition.Agent.Frontmatter.Model)
+	}
+	if len(definition.Agent.Frontmatter.Tools) != 2 {
+		t.Fatalf("expected tools to be parsed, got %v", definition.Agent.Frontmatter.Tools)
+	}
+	if definition.Agent.Frontmatter.MaxTurns == nil || *definition.Agent.Frontmatter.MaxTurns != 8 {
+		t.Fatalf("expected maxTurns to be parsed, got %v", definition.Agent.Frontmatter.MaxTurns)
+	}
+	if len(definition.Agent.Frontmatter.Skills) != 2 {
+		t.Fatalf("expected skills to be parsed, got %v", definition.Agent.Frontmatter.Skills)
+	}
+	if len(definition.Agent.Frontmatter.MCPServers) != 1 || definition.Agent.Frontmatter.MCPServers[0] != "github" {
+		t.Fatalf("expected mcpServers to be parsed, got %v", definition.Agent.Frontmatter.MCPServers)
+	}
+	if definition.Agent.Frontmatter.Fields["metadata"] == nil {
+		t.Fatal("expected arbitrary frontmatter fields to remain available")
+	}
+
+	if definition.Soul == nil {
+		t.Fatal("expected SOUL.md to be loaded")
+	}
+	if !strings.Contains(definition.Soul.Content, "Stay precise") {
+		t.Fatalf("expected soul content to be loaded, got %q", definition.Soul.Content)
+	}
+	if definition.Soul.Path != filepath.Join(tmpDir, "SOUL.md") {
+		t.Fatalf("expected default SOUL.md path, got %q", definition.Soul.Path)
+	}
+}
+
+func TestLoadAgentDefinitionFallsBackToLegacyAgentsMarkdown(t *testing.T) {
+	tmpDir := setupWorkspace(t, map[string]string{
+		"AGENTS.md": "# Legacy Agent\nKeep compatibility.",
+		"SOUL.md":   "# Soul\nLegacy soul.",
+	})
+	defer cleanupWorkspace(t, tmpDir)
+
+	cb := NewContextBuilder(tmpDir)
+	definition := cb.LoadAgentDefinition()
+
+	if definition.Source != AgentDefinitionSourceAgents {
+		t.Fatalf("expected source %q, got %q", AgentDefinitionSourceAgents, definition.Source)
+	}
+	if definition.Agent == nil {
+		t.Fatal("expected AGENTS.md to be loaded")
+	}
+	if definition.Agent.RawFrontmatter != "" {
+		t.Fatalf("legacy AGENTS.md should not have frontmatter, got %q", definition.Agent.RawFrontmatter)
+	}
+	if !strings.Contains(definition.Agent.Body, "Keep compatibility") {
+		t.Fatalf("expected legacy body to be preserved, got %q", definition.Agent.Body)
+	}
+	if definition.Soul == nil || !strings.Contains(definition.Soul.Content, "Legacy soul") {
+		t.Fatal("expected default SOUL.md to be loaded for legacy format")
+	}
+}
+
+func TestLoadBootstrapFilesUsesAgentBodyNotFrontmatter(t *testing.T) {
+	tmpDir := setupWorkspace(t, map[string]string{
+		"AGENT.md": `---
+name: pico
+model: codex-mini
+---
+# Agent
+
+Follow the body prompt.
+`,
+		"SOUL.md":     "# Soul\nSpeak plainly.",
+		"IDENTITY.md": "# Identity\nWorkspace identity.",
+	})
+	defer cleanupWorkspace(t, tmpDir)
+
+	cb := NewContextBuilder(tmpDir)
+	bootstrap := cb.LoadBootstrapFiles()
+
+	if !strings.Contains(bootstrap, "Follow the body prompt") {
+		t.Fatalf("expected AGENT.md body in bootstrap, got %q", bootstrap)
+	}
+	if !strings.Contains(bootstrap, "Speak plainly") {
+		t.Fatalf("expected resolved soul content in bootstrap, got %q", bootstrap)
+	}
+	if strings.Contains(bootstrap, "name: pico") {
+		t.Fatalf("bootstrap should not expose raw frontmatter, got %q", bootstrap)
+	}
+	if strings.Contains(bootstrap, "model: codex-mini") {
+		t.Fatalf("bootstrap should not expose raw frontmatter, got %q", bootstrap)
+	}
+	if !strings.Contains(bootstrap, "SOUL.md") {
+		t.Fatalf("expected bootstrap to label SOUL.md, got %q", bootstrap)
+	}
+	if strings.Contains(bootstrap, "Workspace identity") {
+		t.Fatalf("structured bootstrap should ignore IDENTITY.md, got %q", bootstrap)
+	}
+}
+
+func TestStructuredAgentIgnoresIdentityChanges(t *testing.T) {
+	tmpDir := setupWorkspace(t, map[string]string{
+		"AGENT.md":    "# Agent\nFollow the new structure.",
+		"SOUL.md":     "# Soul\nVersion one.",
+		"IDENTITY.md": "# Identity\nLegacy identity.",
+	})
+	defer cleanupWorkspace(t, tmpDir)
+
+	cb := NewContextBuilder(tmpDir)
+
+	promptV1 := cb.BuildSystemPromptWithCache()
+	if strings.Contains(promptV1, "Legacy identity") {
+		t.Fatalf("structured prompt should not include IDENTITY.md, got %q", promptV1)
+	}
+
+	identityPath := filepath.Join(tmpDir, "IDENTITY.md")
+	if err := os.WriteFile(identityPath, []byte("# Identity\nVersion two."), 0o644); err != nil {
+		t.Fatal(err)
+	}
+	future := time.Now().Add(2 * time.Second)
+	if err := os.Chtimes(identityPath, future, future); err != nil {
+		t.Fatal(err)
+	}
+
+	cb.systemPromptMutex.RLock()
+	changed := cb.sourceFilesChangedLocked()
+	cb.systemPromptMutex.RUnlock()
+	if changed {
+		t.Fatal("IDENTITY.md should not invalidate cache for structured agent definitions")
+	}
+
+	promptV2 := cb.BuildSystemPromptWithCache()
+	if promptV1 != promptV2 {
+		t.Fatal("structured prompt should remain stable after IDENTITY.md changes")
+	}
+}
+
+func cleanupWorkspace(t *testing.T, path string) {
+	t.Helper()
+	if err := os.RemoveAll(path); err != nil {
+		t.Fatalf("failed to clean up workspace %s: %v", path, err)
+	}
+}