From 1830 onward Johnson was almost continuously in public office, being alderman (1828–30) and mayor (1830–33) of Greeneville, state representative (1835–37, 1839–41), state senator (1841–43), Congressman (1843–53), governor of Tennessee (1853–57), and U.S. Senator (1857–62). As U.S. Representative and Senator, Johnson was principally interested in securing legislation to make land in the West available to homesteaders. He voted with other Southern legislators on questions concerning slavery, but after Tennessee seceded (June 8, 1861), he remained in the Senate, the only Southerner there. He vigorously supported Abraham Lincoln's administration, and in Mar., 1862, the President appointed him military governor of Tennessee with the rank of brigadier general of volunteers. His ability in filling this difficult position and the fact that he was a Southerner and a war Democrat made him an ideal choice as running mate to Lincoln on the successful Union ticket in 1864.