After the war, Hunter failed to win re-election to the U.S. Senate, but did serve as the treasurer of Virginia (1874–1880) before retiring to his farm.

After fellow Democrat Grover Cleveland was elected President of the United States in 1884, Hunter became the customs collector for the port of Tappahannock until his death.

Educated first by private tutors, R. M. T. Hunter entered the University of Virginia when he was 17, shortly after his father's death, and became one of its first graduates.

Hunter favored annexing Texas and compromise on the Oregon question (opposing the Wilmot Proviso), and led efforts to retrocede the City of Alexandria back to Virginia (removing it from the District of Columbia).

Senator Hunter delivered an address in Richmond supporting states’ rights in 1852, and in the 1857–58 congressional session advocated admitting Kansas under the pro-slavery Lecompton constitution.

Hunter also drafted and sponsored the Tariff of 1857 (which lowered duties) and creation of the bonded-warehouse system, although federal revenues were thereby reduced.

In January 1860, Hunter delivered a speech in favor of slavery and the right of slaveholders to carry their slaves into the territories.

[10] At the first session of the 1860 Democratic National Convention in Charleston, South Carolina, Hunter was a contender for the presidential nomination, but received little support except from the Virginia delegation.

When the convention reconvened in Baltimore, most Southerners withdrew, including Hunter, and Douglas won the party's nomination.

When this and several other similar efforts failed, Hunter quietly urged his own state to pass the ordinance of secession in April 1861.

Voters in parts of Virginia that had not seceded elected Unionist John S. Carlile to fill the rest of Hunter's term.

Hunter served in the Confederate Senate in Richmond, Virginia, until the war's end, and was at times President pro tem.

Hunter met with President Abraham Lincoln and Secretary of State William H. Seward at the Hampton Roads Conference.

Following Lee's surrender, President Lincoln summoned Hunter to confer regarding Virginia's restoration to the Union.

[13] When some suggested late in the war that their slaves could be armed and serve in the Confederate Army to win their freedom, Senator R.M.T.

Hunter vehemently opposed the proposal with a long speech against it, but after the Virginia legislature passed a resolution to the contrary, voted as instructed but with an emphatic protest.

He died near Lloyds, Virginia, in 1887, and was buried at the Garnett family burial ground in Loretto in Essex County.