The current church was built following the Great Fire of 1831, which destroyed much of downtown Fayetteville including the original church building. It features a white stucco exterior and plaster interior with wooden wainscoting. The main seating area has a large center aisle and two smaller side aisles. Rows of pews flank each side of the center aisle and are divided in the middle, seating 4-5 people on each side.
The church seats approximately 350 people. The nave features a gallery across the back and up each side, providing additional seating. The rear portion of this gallery is home to the mahogany pipe array and console of the church's organ and is where the choir is seated during services. Beautiful stained-glass windows, imported from Germany near the turn of the 19th century, are found on all four walls of the church.
There are eight primary windows in the nave – four on each side wall – and three windows in the chance. The windows of the nave depict biblical scenes, including the birth of Christ, while the windows in the chancel depict St. John in the center, flanked by St. Paul to the left and St. Timothy to the right. The church is built in Neogothic style and features twin primary steeples, each surrounded by four smaller steeples, all covered in soldered lead sheeting. The church is listed on the National Registry of Historic Places.