diff --git a/command/agent/config/config.go b/command/agent/config/config.go
index 81e8ff8625..a03dfe39a4 100644
--- a/command/agent/config/config.go
+++ b/command/agent/config/config.go
@@ -1106,6 +1106,9 @@ func parseTemplateConfig(result *Config, list *ast.ObjectList) error {
 
 	templateConfigList := list.Filter(name)
 	if len(templateConfigList.Items) == 0 {
+		result.TemplateConfig = &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		}
 		return nil
 	}
 
diff --git a/command/agent/config/config_test.go b/command/agent/config/config_test.go
index 0a59b4cc9c..f729aec4be 100644
--- a/command/agent/config/config_test.go
+++ b/command/agent/config/config_test.go
@@ -92,6 +92,9 @@ func TestLoadConfigFile_AgentCache(t *testing.T) {
 				ServiceAccountTokenFile: "/tmp/serviceaccount/token",
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address:          "http://127.0.0.1:1111",
 			CACert:           "config_ca_cert",
@@ -197,6 +200,9 @@ func TestLoadConfigDir_AgentCache(t *testing.T) {
 				ServiceAccountTokenFile: "/tmp/serviceaccount/token",
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address:          "http://127.0.0.1:1111",
 			CACert:           "config_ca_cert",
@@ -267,6 +273,9 @@ func TestLoadConfigDir_AutoAuthAndListener(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -330,6 +339,9 @@ func TestLoadConfigDir_VaultBlock(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -397,6 +409,9 @@ func TestLoadConfigFile_AgentCache_NoListeners(t *testing.T) {
 				ServiceAccountTokenFile: "/tmp/serviceaccount/token",
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address:          "http://127.0.0.1:1111",
 			CACert:           "config_ca_cert",
@@ -476,6 +491,9 @@ func TestLoadConfigFile(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -524,6 +542,9 @@ func TestLoadConfigFile_Method_Wrapping(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -563,6 +584,9 @@ func TestLoadConfigFile_Method_InitialBackoff(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -602,6 +626,9 @@ func TestLoadConfigFile_Method_ExitOnErr(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -628,6 +655,9 @@ func TestLoadConfigFile_AgentCache_NoAutoAuth(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -762,6 +792,9 @@ func TestLoadConfigFile_AgentCache_AutoAuth_NoSink(t *testing.T) {
 			UseAutoAuthTokenRaw: true,
 			ForceAutoAuthToken:  false,
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -805,6 +838,9 @@ func TestLoadConfigFile_AgentCache_AutoAuth_Force(t *testing.T) {
 			UseAutoAuthTokenRaw: "force",
 			ForceAutoAuthToken:  true,
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -848,6 +884,9 @@ func TestLoadConfigFile_AgentCache_AutoAuth_True(t *testing.T) {
 			UseAutoAuthTokenRaw: "true",
 			ForceAutoAuthToken:  false,
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -889,6 +928,9 @@ func TestLoadConfigFile_Agent_AutoAuth_APIProxyAllConfig(t *testing.T) {
 			EnforceConsistency:  "always",
 			WhenInconsistent:    "forward",
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -939,6 +981,9 @@ func TestLoadConfigFile_AgentCache_AutoAuth_False(t *testing.T) {
 			UseAutoAuthTokenRaw: "false",
 			ForceAutoAuthToken:  false,
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -973,6 +1018,9 @@ func TestLoadConfigFile_AgentCache_Persist(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -1008,6 +1056,12 @@ func TestLoadConfigFile_TemplateConfig(t *testing.T) {
 				MaxConnectionsPerHost: 10,
 			},
 		},
+		"missing": {
+			"./test-fixtures/config-template_config-missing.hcl",
+			TemplateConfig{
+				MaxConnectionsPerHost: 10,
+			},
+		},
 	}
 
 	for name, tc := range testCases {
@@ -1141,6 +1195,9 @@ func TestLoadConfigFile_Template(t *testing.T) {
 						},
 					},
 				},
+				TemplateConfig: &TemplateConfig{
+					MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+				},
 				Templates: tc.expectedTemplates,
 			}
 
@@ -1237,6 +1294,9 @@ func TestLoadConfigFile_Template_NoSinks(t *testing.T) {
 					},
 					Sinks: nil,
 				},
+				TemplateConfig: &TemplateConfig{
+					MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+				},
 				Templates: tc.expectedTemplates,
 			}
 
@@ -1271,6 +1331,9 @@ func TestLoadConfigFile_Template_WithCache(t *testing.T) {
 			},
 		},
 		Cache: &Cache{},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Templates: []*ctconfig.TemplateConfig{
 			{
 				Source:      pointerutil.StringPtr("/path/on/disk/to/template.ctmpl"),
@@ -1316,6 +1379,9 @@ func TestLoadConfigFile_Vault_Retry(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1361,6 +1427,9 @@ func TestLoadConfigFile_Vault_Retry_Empty(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1396,6 +1465,9 @@ func TestLoadConfigFile_EnforceConsistency(t *testing.T) {
 			EnforceConsistency: "always",
 			WhenInconsistent:   "retry",
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -1425,6 +1497,9 @@ func TestLoadConfigFile_EnforceConsistency_APIProxy(t *testing.T) {
 			EnforceConsistency: "always",
 			WhenInconsistent:   "retry",
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 	}
 
 	config.Prune()
@@ -1468,6 +1543,9 @@ func TestLoadConfigFile_Disable_Idle_Conns_All(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1517,6 +1595,9 @@ func TestLoadConfigFile_Disable_Idle_Conns_Auto_Auth(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1566,6 +1647,9 @@ func TestLoadConfigFile_Disable_Idle_Conns_Templating(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1615,6 +1699,9 @@ func TestLoadConfigFile_Disable_Idle_Conns_Caching(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1664,6 +1751,9 @@ func TestLoadConfigFile_Disable_Idle_Conns_Proxying(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1713,6 +1803,9 @@ func TestLoadConfigFile_Disable_Idle_Conns_Empty(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1768,6 +1861,9 @@ func TestLoadConfigFile_Disable_Idle_Conns_Env(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1824,6 +1920,9 @@ func TestLoadConfigFile_Disable_Keep_Alives_All(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1873,6 +1972,9 @@ func TestLoadConfigFile_Disable_Keep_Alives_Auto_Auth(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1922,6 +2024,9 @@ func TestLoadConfigFile_Disable_Keep_Alives_Templating(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -1971,6 +2076,9 @@ func TestLoadConfigFile_Disable_Keep_Alives_Caching(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -2020,6 +2128,9 @@ func TestLoadConfigFile_Disable_Keep_Alives_Proxying(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -2069,6 +2180,9 @@ func TestLoadConfigFile_Disable_Keep_Alives_Empty(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
@@ -2124,6 +2238,9 @@ func TestLoadConfigFile_Disable_Keep_Alives_Env(t *testing.T) {
 				},
 			},
 		},
+		TemplateConfig: &TemplateConfig{
+			MaxConnectionsPerHost: DefaultTemplateConfigMaxConnsPerHost,
+		},
 		Vault: &Vault{
 			Address: "http://127.0.0.1:1111",
 			Retry: &Retry{
diff --git a/command/agent/config/test-fixtures/config-template_config-missing.hcl b/command/agent/config/test-fixtures/config-template_config-missing.hcl
new file mode 100644
index 0000000000..4673e0c1df
--- /dev/null
+++ b/command/agent/config/test-fixtures/config-template_config-missing.hcl
@@ -0,0 +1,14 @@
+# Copyright (c) HashiCorp, Inc.
+# SPDX-License-Identifier: BUSL-1.1
+
+vault {
+  address = "http://127.0.0.1:1111"
+  retry {
+    num_retries = 5
+  }
+}
+
+template {
+  source      = "/path/on/disk/to/template.ctmpl"
+  destination = "/path/on/disk/where/template/will/render.txt"
+}