diff --git a/includes/class-wc-stripe-customer.php b/includes/class-wc-stripe-customer.php
index b6e5a036c3..20f524cb8c 100644
--- a/includes/class-wc-stripe-customer.php
+++ b/includes/class-wc-stripe-customer.php
@@ -704,32 +704,90 @@ public function get_payment_methods( $payment_method_type ) {
 			return [];
 		}
 
-		$payment_methods = get_transient( self::PAYMENT_METHODS_TRANSIENT_KEY . $payment_method_type . $this->get_id() );
+		return $this->get_all_payment_methods( [ $payment_method_type ] );
+	}
 
-		if ( false === $payment_methods ) {
-			$params   = WC_Stripe_UPE_Payment_Method_Sepa::STRIPE_ID === $payment_method_type ? '?expand[]=data.sepa_debit.generated_from.charge&expand[]=data.sepa_debit.generated_from.setup_attempt' : '';
-			$response = WC_Stripe_API::request(
-				[
+	/**
+	 * Get all payment methods for a customer.
+	 *
+	 * @param string[] $payment_method_types The payment method types to look for using Stripe method IDs. If the array is empty, it implies all payment method types.
+	 * @param int      $limit                The maximum number of payment methods to return. If the value is -1, no limit is applied.
+	 * @return array
+	 */
+	public function get_all_payment_methods( array $payment_method_types = [], int $limit = -1 ) {
+		if ( ! $this->get_id() ) {
+			return [];
+		}
+
+		$cache_key = self::PAYMENT_METHODS_TRANSIENT_KEY . '__all_' . $this->get_id();
+		$all_payment_methods = get_transient( $cache_key );
+
+		if ( false === $all_payment_methods || ! is_array( $all_payment_methods ) ) {
+			$all_payment_methods    = [];
+			$last_payment_method_id = null;
+
+			do {
+				$request_params = [
 					'customer' => $this->get_id(),
-					'type'     => $payment_method_type,
-					'limit'    => 100, // Maximum allowed value.
-				],
-				'payment_methods' . $params,
-				'GET'
-			);
+					'limit'    => 100,
+				];
 
-			if ( ! empty( $response->error ) ) {
-				return [];
-			}
+				if ( $last_payment_method_id ) {
+					$request_params['starting_after'] = $last_payment_method_id;
+				}
 
-			if ( is_array( $response->data ) ) {
-				$payment_methods = $response->data;
-			}
+				$response = WC_Stripe_API::request( $request_params, 'payment_methods', 'GET' );
+
+				if ( ! empty( $response->error ) ) {
+					if (
+						isset( $response->error->code )
+						&& isset( $response->error->param )
+						&& 'customer' === $response->error->param
+						&& 'resource_missing' === $response->error->code
+					) {
+						// If the customer doesn't exist, cache an empty array.
+						set_transient( $cache_key, [], DAY_IN_SECONDS );
+					}
+					return [];
+				}
+
+				if ( ! is_array( $response->data ) || [] === $response->data ) {
+					break;
+				}
+
+				$all_payment_methods = array_merge( $all_payment_methods, $response->data );
+
+				// Reset the last payment method ID so we can paginate correctly.
+				$last_payment_method_id = null;
+				if ( isset( $response->has_more ) && $response->has_more ) {
+					$last_payment_method = end( $response->data );
+
+					if ( $last_payment_method && ! empty( $last_payment_method->id ) ) {
+						$last_payment_method_id = $last_payment_method->id;
+					}
+				}
+			} while ( null !== $last_payment_method_id );
+
+			// Always cache the result without any filters applied.
+			set_transient( $cache_key, $all_payment_methods, DAY_IN_SECONDS );
+		}
+
+		// Note that we only apply the limit and type filters after fetching and caching all payment methods.
+		$filtered_payment_methods = $all_payment_methods;
+		if ( [] !== $payment_method_types ) {
+			$filtered_payment_methods = array_filter(
+				$filtered_payment_methods,
+				function ( $payment_method ) use ( $payment_method_types ) {
+					return in_array( $payment_method->type, $payment_method_types, true );
+				}
+			);
+		}
 
-			set_transient( self::PAYMENT_METHODS_TRANSIENT_KEY . $payment_method_type . $this->get_id(), $payment_methods, DAY_IN_SECONDS );
+		if ( $limit > 0 ) {
+			return array_slice( $filtered_payment_methods, 0, $limit );
 		}
 
-		return empty( $payment_methods ) ? [] : $payment_methods;
+		return $filtered_payment_methods;
 	}
 
 	/**
@@ -837,6 +895,7 @@ public function clear_cache( $payment_method_id = null ) {
 		foreach ( self::STRIPE_PAYMENT_METHODS as $payment_method_type ) {
 			delete_transient( self::PAYMENT_METHODS_TRANSIENT_KEY . $payment_method_type . $this->get_id() );
 		}
+		delete_transient( self::PAYMENT_METHODS_TRANSIENT_KEY . '__all_' . $this->get_id() );
 		// Clear cache for the specific payment method if provided.
 		if ( $payment_method_id ) {
 			WC_Stripe_Database_Cache::delete( 'payment_method_for_source_' . $payment_method_id );
diff --git a/includes/compat/trait-wc-stripe-subscriptions.php b/includes/compat/trait-wc-stripe-subscriptions.php
index 3078684c53..023de3df71 100644
--- a/includes/compat/trait-wc-stripe-subscriptions.php
+++ b/includes/compat/trait-wc-stripe-subscriptions.php
@@ -1016,69 +1016,69 @@ public function maybe_render_subscription_payment_method( $payment_method_to_dis
 		$payment_method_to_display = __( 'N/A', 'woocommerce-gateway-stripe' );
 
 		try {
-			// Retrieve all possible payment methods for subscriptions.
-			foreach ( WC_Stripe_Customer::STRIPE_PAYMENT_METHODS as $payment_method_type ) {
-				foreach ( $stripe_customer->get_payment_methods( $payment_method_type ) as $source ) {
-					if ( $source->id !== $stripe_source_id ) {
-						continue;
-					}
+			// Retrieve all possible payment methods for the customer so we make minimal API calls to Stripe.
+			$customer_payment_methods = $stripe_customer->get_all_payment_methods();
+
+			foreach ( $customer_payment_methods as $source ) {
+				if ( $source->id !== $stripe_source_id ) {
+					continue;
+				}
+
+				// Legacy handling for Stripe Card objects. ref: https://docs.stripe.com/api/cards/object
+				if ( isset( $source->object ) && WC_Stripe_Payment_Methods::CARD === $source->object ) {
+					/* translators: 1) card brand 2) last 4 digits */
+					$payment_method_to_display = sprintf( __( 'Via %1$s card ending in %2$s', 'woocommerce-gateway-stripe' ), ( isset( $source->brand ) ? wc_get_credit_card_type_label( $source->brand ) : __( 'N/A', 'woocommerce-gateway-stripe' ) ), $source->last4 );
+					break;
+				}
 
-					// Legacy handling for Stripe Card objects. ref: https://docs.stripe.com/api/cards/object
-					if ( isset( $source->object ) && WC_Stripe_Payment_Methods::CARD === $source->object ) {
+				switch ( $source->type ) {
+					case WC_Stripe_Payment_Methods::CARD:
 						/* translators: 1) card brand 2) last 4 digits */
-						$payment_method_to_display = sprintf( __( 'Via %1$s card ending in %2$s', 'woocommerce-gateway-stripe' ), ( isset( $source->brand ) ? wc_get_credit_card_type_label( $source->brand ) : __( 'N/A', 'woocommerce-gateway-stripe' ) ), $source->last4 );
+						$payment_method_to_display = sprintf( __( 'Via %1$s card ending in %2$s', 'woocommerce-gateway-stripe' ), ( isset( $source->card->brand ) ? wc_get_credit_card_type_label( $source->card->brand ) : __( 'N/A', 'woocommerce-gateway-stripe' ) ), $source->card->last4 );
+						break 2;
+					case WC_Stripe_Payment_Methods::SEPA_DEBIT:
+						/* translators: 1) last 4 digits of SEPA Direct Debit */
+						$payment_method_to_display = sprintf( __( 'Via SEPA Direct Debit ending in %1$s', 'woocommerce-gateway-stripe' ), $source->sepa_debit->last4 );
+						break 2;
+					case WC_Stripe_Payment_Methods::CASHAPP_PAY:
+						/* translators: 1) Cash App Cashtag */
+						$payment_method_to_display = sprintf( __( 'Via Cash App Pay (%1$s)', 'woocommerce-gateway-stripe' ), $source->cashapp->cashtag );
+						break 2;
+					case WC_Stripe_Payment_Methods::LINK:
+						/* translators: 1) email address associated with the Stripe Link payment method */
+						$payment_method_to_display = sprintf( __( 'Via Stripe Link (%1$s)', 'woocommerce-gateway-stripe' ), $source->link->email );
+						break 2;
+					case WC_Stripe_Payment_Methods::ACH:
+						$payment_method_to_display = sprintf(
+							/* translators: 1) account type (checking, savings), 2) last 4 digits of account. */
+							__( 'Via %1$s Account ending in %2$s', 'woocommerce-gateway-stripe' ),
+							ucfirst( $source->us_bank_account->account_type ),
+							$source->us_bank_account->last4
+						);
+						break 2;
+					case WC_Stripe_Payment_Methods::BECS_DEBIT:
+						$payment_method_to_display = sprintf(
+							/* translators: last 4 digits of account. */
+							__( 'BECS Direct Debit ending in %s', 'woocommerce-gateway-stripe' ),
+							$source->au_becs_debit->last4
+						);
+						break 2;
+					case WC_Stripe_Payment_Methods::ACSS_DEBIT:
+						$payment_method_to_display = sprintf(
+							/* translators: 1) bank name, 2) last 4 digits of account. */
+							__( 'Via %1$s ending in %2$s', 'woocommerce-gateway-stripe' ),
+							$source->acss_debit->bank_name,
+							$source->acss_debit->last4
+						);
+						break 2;
+					case WC_Stripe_Payment_Methods::BACS_DEBIT:
+						/* translators: 1) the Bacs Direct Debit payment method's last 4 numbers */
+						$payment_method_to_display = sprintf( __( 'Via Bacs Direct Debit ending in (%1$s)', 'woocommerce-gateway-stripe' ), $source->bacs_debit->last4 );
+						break 2;
+					case WC_Stripe_Payment_Methods::AMAZON_PAY:
+						/* translators: 1) the Amazon Pay payment method's email */
+						$payment_method_to_display = sprintf( __( 'Via Amazon Pay (%1$s)', 'woocommerce-gateway-stripe' ), $source->billing_details->email ?? '' );
 						break 2;
-					}
-
-					switch ( $source->type ) {
-						case WC_Stripe_Payment_Methods::CARD:
-							/* translators: 1) card brand 2) last 4 digits */
-							$payment_method_to_display = sprintf( __( 'Via %1$s card ending in %2$s', 'woocommerce-gateway-stripe' ), ( isset( $source->card->brand ) ? wc_get_credit_card_type_label( $source->card->brand ) : __( 'N/A', 'woocommerce-gateway-stripe' ) ), $source->card->last4 );
-							break 3;
-						case WC_Stripe_Payment_Methods::SEPA_DEBIT:
-							/* translators: 1) last 4 digits of SEPA Direct Debit */
-							$payment_method_to_display = sprintf( __( 'Via SEPA Direct Debit ending in %1$s', 'woocommerce-gateway-stripe' ), $source->sepa_debit->last4 );
-							break 3;
-						case WC_Stripe_Payment_Methods::CASHAPP_PAY:
-							/* translators: 1) Cash App Cashtag */
-							$payment_method_to_display = sprintf( __( 'Via Cash App Pay (%1$s)', 'woocommerce-gateway-stripe' ), $source->cashapp->cashtag );
-							break 3;
-						case WC_Stripe_Payment_Methods::LINK:
-							/* translators: 1) email address associated with the Stripe Link payment method */
-							$payment_method_to_display = sprintf( __( 'Via Stripe Link (%1$s)', 'woocommerce-gateway-stripe' ), $source->link->email );
-							break 3;
-						case WC_Stripe_Payment_Methods::ACH:
-							$payment_method_to_display = sprintf(
-								/* translators: 1) account type (checking, savings), 2) last 4 digits of account. */
-								__( 'Via %1$s Account ending in %2$s', 'woocommerce-gateway-stripe' ),
-								ucfirst( $source->us_bank_account->account_type ),
-								$source->us_bank_account->last4
-							);
-							break 3;
-						case WC_Stripe_Payment_Methods::BECS_DEBIT:
-							$payment_method_to_display = sprintf(
-								/* translators: last 4 digits of account. */
-								__( 'BECS Direct Debit ending in %s', 'woocommerce-gateway-stripe' ),
-								$source->au_becs_debit->last4
-							);
-							break 3;
-						case WC_Stripe_Payment_Methods::ACSS_DEBIT:
-							$payment_method_to_display = sprintf(
-								/* translators: 1) bank name, 2) last 4 digits of account. */
-								__( 'Via %1$s ending in %2$s', 'woocommerce-gateway-stripe' ),
-								$source->acss_debit->bank_name,
-								$source->acss_debit->last4
-							);
-							break 3;
-						case WC_Stripe_Payment_Methods::BACS_DEBIT:
-							/* translators: 1) the Bacs Direct Debit payment method's last 4 numbers */
-							$payment_method_to_display = sprintf( __( 'Via Bacs Direct Debit ending in (%1$s)', 'woocommerce-gateway-stripe' ), $source->bacs_debit->last4 );
-							break 3;
-						case WC_Stripe_Payment_Methods::AMAZON_PAY:
-							/* translators: 1) the Amazon Pay payment method's email */
-							$payment_method_to_display = sprintf( __( 'Via Amazon Pay (%1$s)', 'woocommerce-gateway-stripe' ), $source->billing_details->email ?? '' );
-							break 3;
-					}
 				}
 			}
 		} catch ( WC_Stripe_Exception $e ) {
diff --git a/includes/payment-tokens/class-wc-stripe-payment-tokens.php b/includes/payment-tokens/class-wc-stripe-payment-tokens.php
index 839d9b9654..9ad2a7a4e6 100644
--- a/includes/payment-tokens/class-wc-stripe-payment-tokens.php
+++ b/includes/payment-tokens/class-wc-stripe-payment-tokens.php
@@ -301,19 +301,18 @@ public function woocommerce_get_customer_upe_payment_tokens( $tokens, $user_id,
 
 			// Retrieve the payment methods for the enabled reusable gateways.
 			$payment_methods = [];
+			$reusable_payment_method_types = array_keys( self::UPE_REUSABLE_GATEWAYS_BY_PAYMENT_METHOD );
+			$active_payment_method_types   = [];
 			if ( $gateway->is_oc_enabled() ) {
-				// For OC, get all available payment method types
-				foreach ( self::UPE_REUSABLE_GATEWAYS_BY_PAYMENT_METHOD as $payment_method_type => $reausable_gateway_id ) {
+				// For Optimized Checkout, get all available payment method types.
+				foreach ( $reusable_payment_method_types as $payment_method_type ) {
 					$payment_method_instance = WC_Stripe_UPE_Payment_Gateway::get_payment_method_instance( $payment_method_type );
 					if ( $payment_method_instance ) {
-						$retrieved_methods = $customer->get_payment_methods( $payment_method_type );
-						if ( ! empty( $retrieved_methods ) ) {
-							$payment_methods[] = $retrieved_methods;
-						}
+						$active_payment_method_types[] = $payment_method_type;
 					}
 				}
 			} else {
-				foreach ( self::UPE_REUSABLE_GATEWAYS_BY_PAYMENT_METHOD as $payment_method_type => $reausable_gateway_id ) {
+				foreach ( $reusable_payment_method_types as $payment_method_type ) {
 					// The payment method type doesn't match the ones we use. Nothing to do here.
 					if ( ! isset( $gateway->payment_methods[ $payment_method_type ] ) ) {
 						continue;
@@ -321,10 +320,11 @@ public function woocommerce_get_customer_upe_payment_tokens( $tokens, $user_id,
 
 					$payment_method_instance = $gateway->payment_methods[ $payment_method_type ];
 					if ( $payment_method_instance->is_enabled() ) {
-						$payment_methods[] = $customer->get_payment_methods( $payment_method_type );
+						$active_payment_method_types[] = $payment_method_type;
 					}
 				}
 			}
+			$payment_methods = $customer->get_all_payment_methods( $active_payment_method_types );
 
 			// Add SEPA if it is disabled and iDEAL or Bancontact are enabled. iDEAL and Bancontact tokens are saved as SEPA tokens.
 			if ( $gateway->is_sepa_tokens_for_other_methods_enabled() ) {
diff --git a/tests/phpunit/WC_Stripe_Payment_Gateway_Test.php b/tests/phpunit/WC_Stripe_Payment_Gateway_Test.php
index 5ff56f4b6c..3c3e2cfcc7 100644
--- a/tests/phpunit/WC_Stripe_Payment_Gateway_Test.php
+++ b/tests/phpunit/WC_Stripe_Payment_Gateway_Test.php
@@ -595,7 +595,7 @@ public function test_render_subscription_payment_method() {
 		$mock_subscription->save();
 
 		// This is the key the customer's payment methods are stored under in the transient.
-		$transient_key = WC_Stripe_Customer::PAYMENT_METHODS_TRANSIENT_KEY . 'cardcus_mock';
+		$transient_key = WC_Stripe_Customer::PAYMENT_METHODS_TRANSIENT_KEY . '__all_cus_mock';
 
 		$mock_payment_method       = new stdClass();
 		$mock_payment_method->id   = 'src_mock';