The First Presbyterian Church in Demopolis was organized by the Tuscaloosa Presbytery on November 1, 1839 with nine member. The congregation erected a brick church building on the northeast corner of the Public Square in 1843, this building was confiscated during the Civil War, after the War the building served as the Margengo County Courthouse for a few years while the county seat was in Demopolis. The 1843 building remains standing is is called Rooster Hall and is used for public meetings by the city.
The congregation built a wood-frame church at the present location in 1869. The church underwent extensive remodeling in 1905 though the original sanctuary was nearly wholly retained. The church underwent other modification over the years including steeple modification in 1936, an eastside addition in 1953 and a northside addition in 1989.
The building is well maintained and continues to serve its congregation.