diff --git a/agent-schema.json b/agent-schema.json
index 3c126ebf8b..731c133a5c 100644
--- a/agent-schema.json
+++ b/agent-schema.json
@@ -48,7 +48,8 @@
     },
     "agents": {
       "type": "object",
-      "description": "Map of agent configurations",
+      "description": "Map of agent configurations. At least one agent is required.",
+      "minProperties": 1,
       "additionalProperties": {
         "$ref": "#/definitions/AgentConfig"
       }
@@ -109,6 +110,9 @@
     }
   },
   "additionalProperties": false,
+  "required": [
+    "agents"
+  ],
   "definitions": {
     "Lifecycle": {
       "type": "object",
diff --git a/docs/configuration/agents/index.md b/docs/configuration/agents/index.md
index 998910e22e..631c5d516b 100644
--- a/docs/configuration/agents/index.md
+++ b/docs/configuration/agents/index.md
@@ -9,6 +9,8 @@ canonical: https://docs.docker.com/ai/docker-agent/configuration/agents/
 
 _Complete reference for defining agents in your YAML configuration._
 
+A configuration must define at least one agent under `agents`.
+
 ## Full Schema
 
 <!-- yaml-lint:skip -->
diff --git a/docs/configuration/overview/index.md b/docs/configuration/overview/index.md
index 253da9dc97..7380c080c4 100644
--- a/docs/configuration/overview/index.md
+++ b/docs/configuration/overview/index.md
@@ -34,7 +34,7 @@ models:
     model: claude-sonnet-4-5
     max_tokens: 64000
 
-# 4. Agents — define AI agents with their behavior
+# 4. Agents — define AI agents with their behavior (at least one is required)
 agents:
   root:
     model: claude
diff --git a/pkg/config/config.go b/pkg/config/config.go
index 2bb42e5e65..d0c464b649 100644
--- a/pkg/config/config.go
+++ b/pkg/config/config.go
@@ -228,6 +228,10 @@ func migrateToLatestConfig(c any, raw []byte) (latest.Config, error) {
 }
 
 func validateConfig(cfg *latest.Config) error {
+	if len(cfg.Agents) == 0 {
+		return errors.New("at least one agent must be configured (add an entry under 'agents')")
+	}
+
 	if err := validateProviders(cfg); err != nil {
 		return err
 	}
diff --git a/pkg/config/doc_yaml_test.go b/pkg/config/doc_yaml_test.go
index 5dd682d00c..7882c1c29c 100644
--- a/pkg/config/doc_yaml_test.go
+++ b/pkg/config/doc_yaml_test.go
@@ -94,13 +94,18 @@ func TestDocYAMLSnippetsAreValid(t *testing.T) {
 }
 
 // looksLikeFullConfig returns true when the parsed YAML value is a map whose
-// keys are all recognized top-level config keys. This avoids schema-validating
-// partial snippets that would trivially fail required-field checks.
+// keys are all recognized top-level config keys AND it declares "agents".
+// The schema requires "agents" at the root, so a snippet lacking it is a
+// partial doc example (e.g. a models/permissions fragment), not a full
+// config, and shouldn't be schema-validated as one.
 func looksLikeFullConfig(v any) bool {
 	m, ok := v.(map[string]any)
 	if !ok || len(m) == 0 {
 		return false
 	}
+	if _, hasAgents := m["agents"]; !hasAgents {
+		return false
+	}
 	for k := range m {
 		if !topLevelConfigKeys[k] {
 			return false
diff --git a/pkg/config/schema_test.go b/pkg/config/schema_test.go
index 476d469d04..d663348ee9 100644
--- a/pkg/config/schema_test.go
+++ b/pkg/config/schema_test.go
@@ -56,6 +56,51 @@ func TestJsonSchemaWorksForExamples(t *testing.T) {
 	}
 }
 
+// TestJsonSchemaRejectsZeroAgents pins the runtime's "at least one agent"
+// invariant (enforced by validateConfig) at the schema level too. Both the
+// root-level "required": ["agents"] and the "agents"."minProperties": 1
+// constraints are needed: without either one, one of these shapes would
+// pass schema validation despite being rejected at runtime.
+func TestJsonSchemaRejectsZeroAgents(t *testing.T) {
+	t.Parallel()
+
+	schemaBytes, err := os.ReadFile(schemaFile)
+	require.NoError(t, err)
+
+	schema, err := gojsonschema.NewSchema(gojsonschema.NewBytesLoader(schemaBytes))
+	require.NoError(t, err)
+
+	tests := []struct {
+		name string
+		yaml string
+	}{
+		{
+			name: "agents omitted entirely",
+			yaml: `version: "12"
+`,
+		},
+		{
+			name: "agents is an empty map",
+			yaml: `version: "12"
+agents: {}
+`,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			t.Parallel()
+
+			var rawJSON any
+			require.NoError(t, yaml.Unmarshal([]byte(tt.yaml), &rawJSON))
+
+			result, err := schema.Validate(gojsonschema.NewRawLoader(rawJSON))
+			require.NoError(t, err)
+			assert.False(t, result.Valid(), "expected schema to reject config with %s", tt.name)
+		})
+	}
+}
+
 // TestSchemaMatchesGoTypes verifies that every JSON-tagged field in the Go
 // config structs has a corresponding property in agent-schema.json (and
 // vice-versa). This prevents the schema from silently drifting out of sync
diff --git a/pkg/config/validation_test.go b/pkg/config/validation_test.go
index 3f6ebbd38f..6da870ff4e 100644
--- a/pkg/config/validation_test.go
+++ b/pkg/config/validation_test.go
@@ -133,6 +133,20 @@ agents:
 	assert.Contains(t, err.Error(), "2")
 }
 
+func TestLoadConfig_RequiresAtLeastOneAgent(t *testing.T) {
+	t.Parallel()
+
+	cfg := `version: "12"
+models:
+  fast:
+    provider: openai
+    model: gpt-4o-mini
+`
+	_, err := Load(t.Context(), NewBytesSource("test", []byte(cfg)))
+	require.Error(t, err)
+	assert.Contains(t, err.Error(), "at least one agent must be configured")
+}
+
 func TestValidSkillsConfiguration(t *testing.T) {
 	t.Parallel()
 
diff --git a/pkg/server/agents_test.go b/pkg/server/agents_test.go
new file mode 100644
index 0000000000..d03d4c5567
--- /dev/null
+++ b/pkg/server/agents_test.go
@@ -0,0 +1,42 @@
+package server
+
+import (
+	"testing"
+
+	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+
+	"github.com/docker/docker-agent/pkg/config/latest"
+)
+
+// TestAgentsAPIEntry_ZeroAgents pins the docker/docker-agent#3588 handler
+// guard directly: agentsAPIEntry must report ok=false (not panic) for a
+// config with no agents, exercising the len(cfg.Agents)==0 check regardless
+// of whether validateConfig also rejects such a config at load time
+// (defense in depth).
+func TestAgentsAPIEntry_ZeroAgents(t *testing.T) {
+	t.Parallel()
+
+	cfg := &latest.Config{}
+
+	require.NotPanics(t, func() {
+		_, ok := agentsAPIEntry("empty", cfg)
+		assert.False(t, ok)
+	})
+}
+
+func TestAgentsAPIEntry_SingleAndMultiAgent(t *testing.T) {
+	t.Parallel()
+
+	single := &latest.Config{Agents: latest.Agents{{Name: "root", Description: "solo"}}}
+	agent, ok := agentsAPIEntry("single", single)
+	require.True(t, ok)
+	assert.False(t, agent.Multi)
+	assert.Equal(t, "solo", agent.Description)
+
+	multi := &latest.Config{Agents: latest.Agents{{Name: "root", Description: "lead"}, {Name: "helper"}}}
+	agent, ok = agentsAPIEntry("multi", multi)
+	require.True(t, ok)
+	assert.True(t, agent.Multi)
+	assert.Equal(t, "lead", agent.Description)
+}
diff --git a/pkg/server/server.go b/pkg/server/server.go
index 6f1c7e3b74..39900f52eb 100644
--- a/pkg/server/server.go
+++ b/pkg/server/server.go
@@ -21,6 +21,7 @@ import (
 
 	"github.com/docker/docker-agent/pkg/api"
 	"github.com/docker/docker-agent/pkg/config"
+	"github.com/docker/docker-agent/pkg/config/latest"
 	"github.com/docker/docker-agent/pkg/echolog"
 	"github.com/docker/docker-agent/pkg/runtime"
 	"github.com/docker/docker-agent/pkg/session"
@@ -157,31 +158,18 @@ func (s *Server) getAgents(c echo.Context) error {
 	for k, agentSource := range s.sm.Sources {
 		slog.Debug("API source", "source", agentSource.Name())
 
-		c, err := config.Load(c.Request().Context(), agentSource)
+		cfg, err := config.Load(c.Request().Context(), agentSource)
 		if err != nil {
 			slog.Error("Failed to load config from API source", "key", k, "error", err)
 			continue
 		}
 
-		desc := c.Agents.First().Description
-
-		switch {
-		case len(c.Agents) > 1:
-			agents = append(agents, api.Agent{
-				Name:        k,
-				Multi:       true,
-				Description: desc,
-			})
-		case len(c.Agents) == 1:
-			agents = append(agents, api.Agent{
-				Name:        k,
-				Multi:       false,
-				Description: desc,
-			})
-		default:
+		agent, ok := agentsAPIEntry(k, cfg)
+		if !ok {
 			slog.Warn("No agents found in config from API source", "key", k)
 			continue
 		}
+		agents = append(agents, agent)
 	}
 
 	slices.SortFunc(agents, func(a, b api.Agent) int {
@@ -191,6 +179,23 @@ func (s *Server) getAgents(c echo.Context) error {
 	return c.JSON(http.StatusOK, agents)
 }
 
+// agentsAPIEntry summarizes a loaded config into the api.Agent listing
+// entry for /api/agents. The len(cfg.Agents)==0 check MUST run before any
+// access to cfg.Agents (e.g. First()), which panics on an empty slice: this
+// guards the handler even though validateConfig already rejects agent-less
+// configs at load time (defense in depth against a bypass or future
+// regression in that check).
+func agentsAPIEntry(name string, cfg *latest.Config) (api.Agent, bool) {
+	if len(cfg.Agents) == 0 {
+		return api.Agent{}, false
+	}
+	return api.Agent{
+		Name:        name,
+		Multi:       len(cfg.Agents) > 1,
+		Description: cfg.Agents.First().Description,
+	}, true
+}
+
 func (s *Server) getAgentConfig(c echo.Context) error {
 	agentID := c.Param("id")
 
diff --git a/pkg/server/server_test.go b/pkg/server/server_test.go
index 92d9c49afb..88b210eeff 100644
--- a/pkg/server/server_test.go
+++ b/pkg/server/server_test.go
@@ -58,6 +58,28 @@ func TestServer_EmptyList(t *testing.T) {
 	assert.Equal(t, "[]\n", string(buf)) // We don't want null, but an empty array
 }
 
+// TestServer_ZeroAgentSource pins the fix for docker/docker-agent#3588:
+// a config source with no agents must never make GET /api/agents panic
+// (latest.Agents.First() panics on an empty slice). Today validateConfig
+// rejects the agent-less config at load time, so the handler's own
+// len(cfg.Agents)==0 guard (agentsAPIEntry) never even gets exercised by
+// this path — the request still yields a clean, empty listing rather than
+// a panic either way.
+func TestServer_ZeroAgentSource(t *testing.T) {
+	t.Parallel()
+
+	ctx := t.Context()
+	lnPath := startServer(t, ctx, prepareAgentsDir(t, "no_agents.yaml", "pirate.yaml"))
+
+	buf := httpGET(t, ctx, lnPath, "/api/agents")
+
+	var agents []api.Agent
+	unmarshal(t, buf, &agents)
+
+	require.Len(t, agents, 1)
+	assert.Contains(t, agents[0].Name, "pirate")
+}
+
 func TestServer_ListSessions(t *testing.T) {
 	t.Parallel()
 
diff --git a/pkg/server/testdata/no_agents.yaml b/pkg/server/testdata/no_agents.yaml
new file mode 100644
index 0000000000..8c0ddab6be
--- /dev/null
+++ b/pkg/server/testdata/no_agents.yaml
@@ -0,0 +1 @@
+version: "12"