diff --git a/command/agent/config_parse.go b/command/agent/config_parse.go
index cf74386f4..389eb2832 100644
--- a/command/agent/config_parse.go
+++ b/command/agent/config_parse.go
@@ -72,6 +72,29 @@ func ParseConfigFile(path string) (*Config, error) {
 		return nil, fmt.Errorf("failed to decode HCL file %s: %w", path, err)
 	}
 
+	// Re-parse the file to extract the multiple Vault configurations, which we
+	// need to parse by hand because we don't have a label on the block
+	root, err := hcl.Parse(buf.String())
+	if err != nil {
+		return nil, fmt.Errorf("failed to parse HCL file %s: %w", path, err)
+	}
+	list, ok := root.Node.(*ast.ObjectList)
+	if !ok {
+		return nil, fmt.Errorf("error parsing: root should be an object")
+	}
+	matches := list.Filter("vault")
+	if len(matches.Items) > 0 {
+		if err := parseVaults(c, matches); err != nil {
+			return nil, fmt.Errorf("error parsing 'vault': %w", err)
+		}
+	}
+	matches = list.Filter("consul")
+	if len(matches.Items) > 0 {
+		if err := parseConsuls(c, matches); err != nil {
+			return nil, fmt.Errorf("error parsing 'consul': %w", err)
+		}
+	}
+
 	// convert strings to time.Durations
 	tds := []durationConversionMap{
 		{"gc_interval", &c.Client.GCInterval, &c.Client.GCIntervalHCL, nil},
@@ -152,6 +175,30 @@ func ParseConfigFile(path string) (*Config, error) {
 		},
 	}
 
+	// Parse durations for Consul and Vault config blocks if provided.
+	//
+	// Since the map of multiple cluster configuration contains a pointer to
+	// the default block we don't need to parse it directly.
+	for name, consulConfig := range c.Consuls {
+		if consulConfig.ServiceIdentity != nil {
+			tds = append(tds, durationConversionMap{
+				fmt.Sprintf("consuls.%s.service_identity.ttl", name), nil, &consulConfig.ServiceIdentity.TTLHCL,
+				func(d *time.Duration) {
+					consulConfig.ServiceIdentity.TTL = d
+				},
+			})
+		}
+
+		if consulConfig.TemplateIdentity != nil {
+			tds = append(tds, durationConversionMap{
+				fmt.Sprintf("consuls.%s.template_identity.ttl", name), nil, &consulConfig.TemplateIdentity.TTLHCL,
+				func(d *time.Duration) {
+					consulConfig.TemplateIdentity.TTL = d
+				},
+			})
+		}
+	}
+
 	// Add enterprise audit sinks for time.Duration parsing
 	for i, sink := range c.Audit.Sinks {
 		tds = append(tds, durationConversionMap{
@@ -164,28 +211,6 @@ func ParseConfigFile(path string) (*Config, error) {
 		return nil, err
 	}
 
-	// Re-parse the file to extract the multiple Vault configurations, which we
-	// need to parse by hand because we don't have a label on the block
-	root, err := hcl.Parse(buf.String())
-	if err != nil {
-		return nil, fmt.Errorf("failed to parse HCL file %s: %w", path, err)
-	}
-	list, ok := root.Node.(*ast.ObjectList)
-	if !ok {
-		return nil, fmt.Errorf("error parsing: root should be an object")
-	}
-	matches := list.Filter("vault")
-	if len(matches.Items) > 0 {
-		if err := parseVaults(c, matches); err != nil {
-			return nil, fmt.Errorf("error parsing 'vault': %w", err)
-		}
-	}
-	matches = list.Filter("consul")
-	if len(matches.Items) > 0 {
-		if err := parseConsuls(c, matches); err != nil {
-			return nil, fmt.Errorf("error parsing 'consul': %w", err)
-		}
-	}
 	// report unexpected keys
 	err = extraKeys(c)
 	if err != nil {
diff --git a/command/agent/config_parse_test.go b/command/agent/config_parse_test.go
index 0fdd05919..5ffdd9568 100644
--- a/command/agent/config_parse_test.go
+++ b/command/agent/config_parse_test.go
@@ -240,11 +240,15 @@ var basicConfig = &Config{
 			Audience: []string{"consul.io", "nomad.dev"},
 			Env:      pointer.Of(false),
 			File:     pointer.Of(true),
+			TTL:      pointer.Of(1 * time.Hour),
+			TTLHCL:   "1h",
 		},
 		TemplateIdentity: &config.WorkloadIdentityConfig{
 			Audience: []string{"consul.io"},
 			Env:      pointer.Of(true),
 			File:     pointer.Of(false),
+			TTL:      pointer.Of(2 * time.Hour),
+			TTLHCL:   "2h",
 		},
 	},
 	Consuls: map[string]*config.ConsulConfig{
@@ -276,11 +280,15 @@ var basicConfig = &Config{
 				Audience: []string{"consul.io", "nomad.dev"},
 				Env:      pointer.Of(false),
 				File:     pointer.Of(true),
+				TTL:      pointer.Of(1 * time.Hour),
+				TTLHCL:   "1h",
 			},
 			TemplateIdentity: &config.WorkloadIdentityConfig{
 				Audience: []string{"consul.io"},
 				Env:      pointer.Of(true),
 				File:     pointer.Of(false),
+				TTL:      pointer.Of(2 * time.Hour),
+				TTLHCL:   "2h",
 			},
 		},
 	},
diff --git a/command/agent/testdata/basic.hcl b/command/agent/testdata/basic.hcl
index 14c784db5..c1dc20e6a 100644
--- a/command/agent/testdata/basic.hcl
+++ b/command/agent/testdata/basic.hcl
@@ -248,11 +248,13 @@ consul {
     aud  = ["consul.io", "nomad.dev"]
     env  = false
     file = true
+    ttl  = "1h"
   }
   template_identity {
     aud  = ["consul.io"]
     env  = true
     file = false
+    ttl  = "2h"
   }
 }
 
diff --git a/command/agent/testdata/basic.json b/command/agent/testdata/basic.json
index baabdc528..9f05fede2 100644
--- a/command/agent/testdata/basic.json
+++ b/command/agent/testdata/basic.json
@@ -173,7 +173,8 @@
           "nomad.dev"
         ],
         "env": false,
-        "file": true
+        "file": true,
+        "ttl": "1h"
       },
       "ssl": true,
       "template_identity": {
@@ -181,7 +182,8 @@
           "consul.io"
         ],
         "env": true,
-        "file": false
+        "file": false,
+        "ttl": "2h"
       },
       "timeout": "5s",
       "token": "token1",
diff --git a/nomad/config.go b/nomad/config.go
index 68a45e67e..116ce70d2 100644
--- a/nomad/config.go
+++ b/nomad/config.go
@@ -508,6 +508,9 @@ func workloadIdentityFromConfig(widConfig *config.WorkloadIdentityConfig) *struc
 	if widConfig.File != nil {
 		wid.File = *widConfig.File
 	}
+	if widConfig.TTL != nil {
+		wid.TTL = *widConfig.TTL
+	}
 
 	return wid
 }
diff --git a/nomad/structs/config/consul_test.go b/nomad/structs/config/consul_test.go
index 2a9f451da..7f6c666d2 100644
--- a/nomad/structs/config/consul_test.go
+++ b/nomad/structs/config/consul_test.go
@@ -99,6 +99,7 @@ func TestConsulConfig_Merge(t *testing.T) {
 			Audience: []string{"consul.io", "nomad.dev"},
 			Env:      pointer.Of(false),
 			File:     pointer.Of(true),
+			TTL:      pointer.Of(2 * time.Hour),
 		},
 		ExtraKeysHCL: []string{"b", "2"},
 	}
@@ -134,6 +135,7 @@ func TestConsulConfig_Merge(t *testing.T) {
 			Audience: []string{"consul.io", "nomad.dev"},
 			Env:      pointer.Of(false),
 			File:     pointer.Of(true),
+			TTL:      pointer.Of(2 * time.Hour),
 		},
 		ExtraKeysHCL: []string{"a", "1"}, // not merged
 	}
diff --git a/nomad/structs/config/workload_id.go b/nomad/structs/config/workload_id.go
index 664209c98..135668c0b 100644
--- a/nomad/structs/config/workload_id.go
+++ b/nomad/structs/config/workload_id.go
@@ -5,6 +5,7 @@ package config
 
 import (
 	"slices"
+	"time"
 
 	"github.com/hashicorp/go-set"
 	"github.com/hashicorp/nomad/helper/pointer"
@@ -31,6 +32,11 @@ type WorkloadIdentityConfig struct {
 	// File writes the Workload Identity into the Task's secrets directory
 	// if set.
 	File *bool `mapstructure:"file"`
+
+	// TTL is used to determine the expiration of the credentials created for
+	// this identity (eg the JWT "exp" claim).
+	TTL    *time.Duration `mapstructure:"-"`
+	TTLHCL string         `mapstructure:"ttl" json:"-"`
 }
 
 func (wi *WorkloadIdentityConfig) Copy() *WorkloadIdentityConfig {
@@ -68,6 +74,12 @@ func (wi *WorkloadIdentityConfig) Equal(other *WorkloadIdentityConfig) bool {
 	if !pointer.Eq(wi.File, other.File) {
 		return false
 	}
+	if !pointer.Eq(wi.TTL, other.TTL) {
+		return false
+	}
+	if wi.TTLHCL != other.TTLHCL {
+		return false
+	}
 
 	return true
 }
@@ -94,6 +106,10 @@ func (wi *WorkloadIdentityConfig) Merge(other *WorkloadIdentityConfig) *Workload
 
 	result.Env = pointer.Merge(result.Env, other.Env)
 	result.File = pointer.Merge(result.File, other.File)
+	result.TTL = pointer.Merge(result.TTL, other.TTL)
+	if other.TTLHCL != "" {
+		result.TTLHCL = other.TTLHCL
+	}
 
 	return result
 }
diff --git a/nomad/structs/config/workload_id_test.go b/nomad/structs/config/workload_id_test.go
index d3cbc12c3..6602fff11 100644
--- a/nomad/structs/config/workload_id_test.go
+++ b/nomad/structs/config/workload_id_test.go
@@ -5,6 +5,7 @@ package config
 
 import (
 	"testing"
+	"time"
 
 	"github.com/hashicorp/nomad/ci"
 	"github.com/hashicorp/nomad/helper/pointer"
@@ -19,6 +20,7 @@ func TestWorkloadIdentityConfig_Copy(t *testing.T) {
 		Audience: []string{"aud"},
 		Env:      pointer.Of(true),
 		File:     pointer.Of(false),
+		TTL:      pointer.Of(time.Hour),
 	}
 
 	// Verify Copy() returns the same values but different pointer.
@@ -31,6 +33,7 @@ func TestWorkloadIdentityConfig_Copy(t *testing.T) {
 	clone.Audience = []string{"aud", "clone"}
 	clone.Env = pointer.Of(false)
 	clone.File = pointer.Of(true)
+	clone.TTL = pointer.Of(time.Second)
 
 	must.NotEq(t, original, clone)
 	must.NotEqOp(t, original, clone)
@@ -52,12 +55,14 @@ func TestWorkloadIdentityConfig_Equal(t *testing.T) {
 				Audience: []string{"aud"},
 				Env:      pointer.Of(true),
 				File:     pointer.Of(false),
+				TTL:      pointer.Of(time.Hour),
 			},
 			b: &WorkloadIdentityConfig{
 				Name:     "test",
 				Audience: []string{"aud"},
 				Env:      pointer.Of(true),
 				File:     pointer.Of(false),
+				TTL:      pointer.Of(time.Hour),
 			},
 			expectEq: true,
 		},
@@ -121,6 +126,16 @@ func TestWorkloadIdentityConfig_Equal(t *testing.T) {
 			},
 			expectEq: false,
 		},
+		{
+			name: "different ttl",
+			a: &WorkloadIdentityConfig{
+				TTL: pointer.Of(time.Hour),
+			},
+			b: &WorkloadIdentityConfig{
+				TTL: pointer.Of(time.Minute),
+			},
+			expectEq: false,
+		},
 	}
 
 	for _, tc := range testCases {
@@ -152,6 +167,7 @@ func TestWorkloadIdentityConfig_Merge(t *testing.T) {
 				Audience: []string{"aud"},
 				Env:      pointer.Of(true),
 				File:     pointer.Of(false),
+				TTL:      pointer.Of(time.Hour),
 			},
 		},
 		{
@@ -164,6 +180,7 @@ func TestWorkloadIdentityConfig_Merge(t *testing.T) {
 				Audience: []string{"aud", "other"},
 				Env:      pointer.Of(true),
 				File:     pointer.Of(false),
+				TTL:      pointer.Of(time.Hour),
 			},
 		},
 		{
@@ -176,6 +193,7 @@ func TestWorkloadIdentityConfig_Merge(t *testing.T) {
 				Audience: []string{"aud"},
 				Env:      pointer.Of(false),
 				File:     pointer.Of(false),
+				TTL:      pointer.Of(time.Hour),
 			},
 		},
 		{
@@ -188,6 +206,20 @@ func TestWorkloadIdentityConfig_Merge(t *testing.T) {
 				Audience: []string{"aud"},
 				Env:      pointer.Of(true),
 				File:     pointer.Of(true),
+				TTL:      pointer.Of(time.Hour),
+			},
+		},
+		{
+			name: "merge ttl",
+			other: &WorkloadIdentityConfig{
+				TTL: pointer.Of(time.Second),
+			},
+			expected: &WorkloadIdentityConfig{
+				Name:     "test",
+				Audience: []string{"aud"},
+				Env:      pointer.Of(true),
+				File:     pointer.Of(false),
+				TTL:      pointer.Of(time.Second),
 			},
 		},
 	}
@@ -199,6 +231,7 @@ func TestWorkloadIdentityConfig_Merge(t *testing.T) {
 				Audience: []string{"aud"},
 				Env:      pointer.Of(true),
 				File:     pointer.Of(false),
+				TTL:      pointer.Of(time.Hour),
 			}
 			got := original.Merge(tc.other)
 			must.Eq(t, tc.expected, got)