|Stephen Elliott, Jr.||1841–1845|
|Rufus M. White||1845–1853|
|George H. Clark||1853–1861|
|Cameron Farquhar McRae||1862–1867|
|Charles Hall Strong||1878–1914|
|William T. Dakin||1914–1923|
|William Aimison Jonnard||1924–1929|
|Charles C. J. Carpenter||1929–1936|
|Paul W. Pritchartt||1970–1973|
|William H. Ralston, Jr.||1974–1998|
|Michael L. Carreker||1998–2006|
|Gavin G. Dunbar||2006–present|
The church was formed in 1841 from the growing Christ Church, Savannah, as part of a plan to increase Episcopal presence in Georgia and to provide for a first bishop of the diocese. One of its founders was local businessman Edward Padelford. After his death in 1870, his name was added to one of the church's stained-glass windows. Eleven other windows are also dedicated to notable early members of the church.
St. John's first building was consecrated in 1843. When the congregation outgrew this building, the construction was undertaken of the current building (which is situated in Madison Square, across from the historic Green-Meldrim House, now the church's parish house). The building was designed by Calvin N. Otis of Buffalo, New York, and was consecrated in May 1853.
The Parish continues to use the 1928 Book of Common Prayer, as the basis for worship. St. John's maintains a cordial relationship with the Episcopal Diocese of Georgia, although the character of the congregation is more traditional than most of the parishes in The Episcopal Church (TEC).
- Linton Weeks. St. John's Church in Savannah. 1985.