diff --git a/CHANGELOG.md b/CHANGELOG.md
index 5ab1897..84f704d 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -13,6 +13,7 @@
 - Re-worked the OIDC integration to adhere to the correct standards and surface more errors to the user.
     - Deprecated `oidc.redirect_uri` and automated callback URL detection in favor of setting `server.base_url` correctly.
     - Explicitly added `oidc.use_pkce` to correctly determine PKCE configuration.
+    - `oidc.token_endpoint_auth_method` is now optional and will attempt to be auto-detected, defaulting to `client_secret_basic` if unavailable (closes [#410](https://github.com/tale/headplane/issues/410)).
 - Removed several unnecessarily verbose or spammy log messages.
 - Updated the minimum Docker API used to support the latest Docker versions (via [#370](https://github.com/tale/headplane/pull/370)).
 - Enhanced the node tag dialog to show a dropdown of assignable tags (via [#362](https://github.com/tale/headplane/pull/362)).
diff --git a/app/server/config/config-schema.ts b/app/server/config/config-schema.ts
index 8a6e71b..bc3e79b 100644
--- a/app/server/config/config-schema.ts
+++ b/app/server/config/config-schema.ts
@@ -101,13 +101,12 @@ const oidcConfig = type({
 	authorization_endpoint: 'string.url?',
 	token_endpoint: 'string.url?',
 	userinfo_endpoint: 'string.url?',
+	token_endpoint_auth_method:
+		'"client_secret_basic" | "client_secret_post" | "client_secret_jwt"?',
 
 	// Old/deprecated options
 	user_storage_file: 'string.lower = "/var/lib/headplane/users.json"',
 	strict_validation: type('unknown').narrow(deprecatedField()).optional(),
-	token_endpoint_auth_method: type('unknown')
-		.narrow(deprecatedField())
-		.optional(),
 });
 
 const partialOidcConfig = type({
@@ -125,13 +124,12 @@ const partialOidcConfig = type({
 	authorization_endpoint: 'string.url?',
 	token_endpoint: 'string.url?',
 	userinfo_endpoint: 'string.url?',
+	token_endpoint_auth_method:
+		'"client_secret_basic" | "client_secret_post" | "client_secret_jwt"?',
 
 	// Old/deprecated options
 	user_storage_file: 'string.lower?',
 	strict_validation: type('unknown').narrow(deprecatedField()).optional(),
-	token_endpoint_auth_method: type('unknown')
-		.narrow(deprecatedField())
-		.optional(),
 });
 
 const agentConfig = type({
diff --git a/app/server/web/oidc-connector.ts b/app/server/web/oidc-connector.ts
index 9a00f8f..bee4c57 100644
--- a/app/server/web/oidc-connector.ts
+++ b/app/server/web/oidc-connector.ts
@@ -208,7 +208,53 @@ async function discoveryCoalesce(
 		},
 		config.client_id,
 		config.client_secret,
+		negotiateTokenEndpointAuthMethod(config, metadata),
 	);
 
 	return oidcClient;
 }
+
+/**
+ * Determines the token endpoint authentication method based on config and metadata.
+ *
+ * @param config The OIDC configuration.
+ * @param metadata The OIDC server metadata.
+ * @returns The client authentication method for the token endpoint.
+ */
+function negotiateTokenEndpointAuthMethod(
+	config: OidcConfig,
+	metadata: oidc.ServerMetadata,
+): oidc.ClientAuth {
+	if (config.token_endpoint_auth_method != null) {
+		switch (config.token_endpoint_auth_method) {
+			case 'client_secret_basic':
+				return oidc.ClientSecretBasic(config.client_secret);
+			case 'client_secret_post':
+				return oidc.ClientSecretPost(config.client_secret);
+			case 'client_secret_jwt':
+				return oidc.ClientSecretJwt(config.client_secret);
+		}
+	}
+
+	const supported = metadata.token_endpoint_auth_methods_supported;
+	if (supported != null && supported.length > 0) {
+		// Prefer client_secret_basic (spec default), otherwise use first available
+		if (supported.includes('client_secret_basic')) {
+			return oidc.ClientSecretBasic(config.client_secret);
+		}
+
+		if (supported.includes('client_secret_post')) {
+			return oidc.ClientSecretPost(config.client_secret);
+		}
+
+		if (supported.includes('client_secret_jwt')) {
+			return oidc.ClientSecretJwt(config.client_secret);
+		}
+	}
+
+	log.warn(
+		'config',
+		'Falling back to client_secret_basic for token endpoint authentication',
+	);
+	return oidc.ClientSecretBasic(config.client_secret);
+}
diff --git a/config.example.yaml b/config.example.yaml
index 6952e91..0ab2d31 100644
--- a/config.example.yaml
+++ b/config.example.yaml
@@ -185,6 +185,11 @@ integration:
   # token_endpoint: ""
   # userinfo_endpoint: ""
 
+  # The authentication method to use when communicating with the token endpoint.
+  # This is fully optional and Headplane will attempt to auto-detect the best
+  # method and fall back to `client_secret_basic` if unsure.
+  # token_endpoint_auth_method: "client_secret_post"
+
   # The client ID for the OIDC client
   # For the best experience please ensure this is *identical* to the client_id
   # you are using for Headscale. because