Built from 1839 to 1842 by Bishop Leonidas Polk, it was an active church in the Antebellum South.

[2][3] One of his sons, Leonidas Polk, served as the rector of St. John's Episcopal Church, which was based in his own house, Ashwood Hall, from January 1, 1834 to August 9, 1838.

[2][3] It was built where once stood a tall cherry tree, which was felled and used to make wood structures inside the churches such as the balcony or the reredos.

[2] Mary Elizabeth Martin, Gideon Johnson Pillow's wife, and their son, attended services.

[4] On March 31, 1862, in the midst of the American Civil War of 1861-1865, Union Brigadier General Don Carlos Buell broke into the church building and ransacked it, breaking the window glasses.

[2] Days before the Battle of Franklin of November 30, 1864, General Patrick Cleburne (1828–1864) was passing by St. John's and he remarked to his aides something like, "This is such a beautiful church that it would almost be worth dying so one could be buried here.