Commissioned in 1864, the ship spent her entire active career with the James River Flotilla covering the water approaches to the Confederate States capital of Richmond, Virginia, although her only notable engagement was the Battle of Trent's Reach.

After the war, she was purchased by France where she served as a coastal defense ship in the French Navy (Marine Nationale).

A 5-by-15-inch (127 by 381 mm) soft iron band was fitted around the base of the turrets to prevent shells and fragments from jamming them as had happened during the First Battle of Charleston Harbor in April 1863.

[9] Construction was delayed by shortages of material, labor and the closing of the shipyard during the New York City draft riots in July 1863.

[2] Escorted by the gunboat USS Mattabesett, the ship departed New York City on 21 April and arrived at Hampton Roads in Union-occupied Virginia two days later.

Assigned to the James River Flotilla, she supported General Ulysses S. Grant's drive on Richmond, Virginia.

[1] Early in January 1865, most of the Union ironclads were withdrawn from the James River as Rear Admiral David D. Porter assembled most of his ships for the forthcoming attack on Fort Fisher, North Carolina.

[10] When the Confederate squadron steamed down river to attack the weakened Union forces, Onondaga dropped downstream to a position where she could maneuver more easily.

[11] The squadron commander, Flag Officer John K. Mitchell, recalled them several hours later and ordered them to anchor further upstream under the guns of Battery Dantzler.

As the Confederate ships were refloated at 10:45, Onondaga approached the Union obstructions and opened fire at an estimated range of 880 yards (800 m).

[13] Onondaga continued to support Union troops for the rest of the war and steamed north after its end on 9 April.

[3] Other alterations included reworking her hull sides with teak backing the armor, a larger rudder and, probably, removal of the rings around the propellers.