He studied law, was admitted to the Virginia State Bar, and opened a practice in Lexington in 1839.

Although never a true abolitionist, he signed the Ruffner Pamphlet of 1847, which proposed the abolition of slavery in that part of Virginia west of the Blue Ridge Mountains; however, he soon repudiated this antislavery stand.

John Letcher was elected as Governor of Virginia in 1859, defeating Whig candidate William L. Goggin, and served from 1860 to 1864: In accepting the nomination he states "in language distinct and emphatic, that he regards the institution of slavery, existing in Virginia and other slave States, as morally, socially and politically right."

[1]Letcher was prominent in the organization of the Peace Conference of 1861 that met in Washington, D.C., on February 8, 1861, to devise means to prevent the impending American Civil War.

[5] Colonel John Brown Baldwin defeated Letcher in May 1863 for a seat in the Second Confederate Congress.

1859 – Letcher was elected Governor of Virginia, defeating American William Leftwich Goggin.