The railroad was conceived and financed by leading cottonplanters who needed a way to get their crop to textile mills in England and New England. It was also used by naval stores merchants and timber interests of the area to transport their goods to East Coast ports. The Tallahassee Railroad Company was approved in 1835 by the Florida Territorial Legislative Council. Also that year, the Tallahassee Railroad Company received the first federalland grant to a railroad. In 1835 construction began on the Tallahassee-St. Marks Railroad. The railroad was completed in 1837 and began operation that year. It was a mule-drawn railroad with wooden rails that connected Tallahassee, Florida, then the territorial capitol, with the Gulf port of St. Marks — a distance of. By 1839 the railroad was extended south to Port Leon. In 1843, Port Leon was destroyed by a massive hurricane. The railroad terminal there was moved back to St. Marks. In 1856, the wooden rails were replaced by steel rails, and mules by steam locomotives. During the Civil War, the Confederates used the railroad extensively to move troops, artillery and supplies in defense of Tallahassee. In March 1865, the railroad achieved its highest military significance when it was used to deploy Confederate troops quickly south from Tallahassee in the face of an advance by Union troops. The railroad enabled Generals Samuel Jones and William Miller to put enough men into place to defeat Union General John Newton at the Battle of Natural Bridge on March 6, 1865. In 1880, the railroad began to transport naval stores and timber for Leon County's logging industry. In 1983, the Seaboard Railroad filed to abandon the line between Capital Circle in Tallahassee and St. Marks. The Tallahassee-St. Marks railway line has the historical distinction of being the longest-operating railroad in Florida and served the area for 147 years. Francis de Laporte de Castelnau called it "the worst that has yet been built in the entire world." In 1984 the corridor was purchased by the Florida Department of Transportation. The Florida Park Service currently maintains it as the Tallahassee-St. Marks Historic Railroad State Trail.
