The vessel was assigned to the James River Flotilla of the North Atlantic Blockading Squadron upon completion in September 1864.

She engaged Confederate artillery batteries during the year and later participated in both the first and second battles of Fort Fisher, defending the approaches to Wilmington, North Carolina, in December 1864 – January 1865.

Mahopac returned to the James River after the capture of Fort Fisher and remained there until Richmond, Virginia was occupied in early April.

A few days later, the monitor was transferred to Washington, D.C. and decommissioned in June and recommissioned in early 1866 for service on the East Coast and in the Caribbean.

[4] The exposed sides of the hull were protected by five layers of one-inch (25 mm) wrought iron plates, backed by wood.

A "rifle screen" of 1⁄2-inch (13 mm) armor three feet (0.9 m) high was installed on the top of the turret to protect the crew against Confederate snipers based on a suggestion by Commander Tunis A. M. Craven, captain of her sister ship Tecumseh.

After Butler ordered his men re-embarked onto their transports on 26 December, the monitor was towed to Beaufort by the gunboat Fort Jackson.

Together with Canonicus and Saugus, the double-turreted monitor Onondaga and the armored frigate New Ironsides, she bombarded the fort for three days until it was captured by Union troops.

Despite the loss of one gun, the ship fired 204 shells at the fort; she was hit several times in return, but suffered neither damage nor casualties.

[14] The ship remained there on picket duty until 8 March when she returned to Chesapeake Bay[6] and rejoined the North Atlantic Blockading Squadron.

She contributed boats for clearing the James River of "torpedoes" after the Confederate ships were scuttled on the night of 2/3 April and Richmond occupied.