In 1826, Dix married Catherine Morgan, the adopted daughter of Congressman John J. Morgan, who gave Dix a job overseeing his upstate New York land holdings in Cooperstown. John and Catherine moved to Cooperston in 1828, and John practiced law in addition to overseeing the land holdings. Also, Dix was appointed Adjutant General of New York State by Governor Throop, and he served as Secretary of State for New York.
During the Civil War, as a member of the Union army, he commanded the Department of Virginia from June, 1862 until July, 1863, and the Department of the East from July, 1863 until April, 1865.
Dix died in New York City.