After the war he attended the Fort Edward Collegiate Institute and graduated in 1864.
During the American Civil War enlisted as a Private in Company C, 16th New York Volunteer Infantry Regiment on April 27, 1861. He served until he was mustered out with the regiment on May 18, 1863. In 1866 he worked as the deputy collector of customs at Rouses Point, New York until 1872.
After that he engaged in the manufacture of charcoal bloom iron in the Saranac hamlet of Moffitsville and in Belmont, Franklin (now Allegany) County, from 1872–1891.
John Moffitt was elected as a Republican to the Fiftieth and Fifty-first Congresses (March 4, 1887 - March 3, 1891) but he was not a candidate for renomination in 1890. After leaving Congress he was a manager of the Syracuse Street Railway Company from 1891–1899 and superintendent of the city water department from 1900 to 1902.
He then moved to Plattsburgh to become Cashier of the Plattsburgh National Bank, of which he became President in 1904. He was also a delegate to the 1912 Republican National Convention.
John Moffitt died in Plattsburgh, and is buried in Plattsburgh"s Mount Carmel Cemetery.
In 1877 he was elected Saranac"s Town Supervisor, which also made him a member of the Clinton County Board of Supervisors. Moffitt remained active in Republican politics as Chairman of the Clinton County Republican Committee and a member of the New York Republican State Committee.