The City of Folkston serves as the county seat for Charlton County. It is governed by a mayor and five council members. Both the mayor and council serve four-year terms.
The City of Folkston is divided into two districts (District 1 and District 2) with two council members serving in each district and one council member serving at large. The day-to-day operations are managed by the city manager, who reports to the mayor and council.
Along with the city manager, the city clerk manages the city's finance and human resource operations. The city attorney provides legal counsel to the mayor, council, and city manager and represents the City of Folkston in all legal matters.