The land on which the church sits was donated by Cornelius Keith, the earliest settler in the area. Keith arrived in 1743 and formed a treaty with Cherokee Chief Woolenoy. It is the Anglicized version of Woolenoy gives the church its name. According to legend, the cemetery was originally a Cherokee burial ground. The area was inhabited almost entirely by Cherokee until after the American Revolution.
By 1795, there were enough white settlers in the Pumpkintown area to establish a church. The Reverend John Chastain established Woolenoy Bapist Church, and in 1827, the name was changed to Oolenoy. The first church to occupy the spot was a simple log building, which was followed by a larger frame building in the late 1800s, and the current building, which was constructed in 1952.
The cemetery, which is considered a fine example of early nineteenth century burials, with many fine examples of funerary art, contains more than 800 marked graves. These include the graves of slaves, numerous veterans of the American Revolution, and some of the area's earliest settlers, including the Keith family.
The cemetery (though not the church building itself) is listed on the National Register of Historic Places, and occasional burials still take place there.