[1] A Democrat, Milligan was elected to the Tennessee House of Representatives for three terms, from 1841 to 1846 (24th, 25th, and 26th General Assemblies).

[2][1] During his time in the state legislature, Milligan developed a close friendship with future President Andrew Johnson.

[1] He was appointed Inspector General of the state militia by then-Governor Johnson in 1853,[3] and represented Tennessee on a commission to resolve a boundary dispute with Virginia in 1858.

[4][1] He was a delegate to the Peace Conference of 1861 in Washington, D.C.[1] During the American Civil War, he remained loyal to the Union,[2] and was present at the pro-Union East Tennessee Convention in April 1864.

Of this group, Milligan is described as one of only two "who were men of talent, and were good lawyers", the other being George Andrews.