In 1847, Fauntleroy began private practice in Winchester and in 1850 was elected
Commonwealth's Attorney for
Frederick County. In 1860, he owned four slaves (65 and 25 year old Black women and 2 and 5-year-old girls). Frederick county voters twice elected Fauntleroy as one of their delegates in the
Virginia General Assembly, so he served (part-time) from 1857 to 1859 and again in 1877. In the prewar election, he and
M. R. Kaufman ousted the two previous delegates, and the following term,
George W. Ward received the most votes and was seated alongside Kaufman. As the American Civil War began, the elder Fauntleroy gave up his U.S. Army commission and returned to Virginia, where he lived with this son. He had accepted a commission as general in the Virginia militia, but not a Confederate States Army commission, unlike two of his sons (this Fauntleroy's brothers). His eldest son C. M. Fauntleroy also resigned his U.S. Navy commission, but the ship he commanded, the
CSS Rappahannock, was never permitted to leave European waters. His brother Dr. Archibald Magill Fauntleroy served as a Confederate surgeon. Despite health problems following the Civil War, after agreeing not to again own enslaved people and receiving a presidential pardon on September 29, 1865, Fauntleroy resumed his legal practice and political career. In 1877, Fauntleroy and Nimrod Whitacre ousted the previous men representing Frederick County in the Virginia House of Delegates, but after subsequent redistricting,
Edmund P. Dandridge became the sole representative of Winchester and Frederick County. In 1879 Fauntleroy became the
Secretary of the Commonwealth of Virginia, a position appointed by the Governor. In 1882, the
Readjuster Party had taken control of the state legislature, and refused to renew the 12-year terms of members of the
Supreme Court of Appeals (all but one selected immediately after Virginia voters accepted a new state constitution after the Civil War which prohibited slavery) and elected four members effective January 1, 1883. Fauntleroy,
Benjamin W. Lacy,
Drury A. Hinton and
Robert A. Richardson served together on the appellate bench for their twelve-year terms until again the legislature (now controlled by the Democratic Party) refused to renew their terms, so five successors took office in January 1895.(thus the succession box above is arbitrary) ==Later life and death==