Her first war service began 31 July 1861 when she sailed for Kingston, Jamaica, to search for the elusive Confederate raider Sumter commanded by Raphael Semmes.

Departing 25 August, Richmond arrived at Key West on 2 September, then proceeded north to join the Gulf Blockading Squadron.

In the early morning darkness of the 12th, the Confederate ram Manassas and three armed steamers of Commodore Hollins's Mosquito Fleet attacked Richmond and her consorts in an attempt to break the blockade in what became the Battle of the Head of Passes.

Fortunately, the Army transport, McClellan, arrived with long range rifled guns on loan from Fort Pickens; and halted the second Confederate attack.

Richmond then cruised off the mouth of the river, blockading Confederate forces and aiding Army engineers erecting batteries on the banks of the South and Southwest passages.

One shell hit forward, destroying railing and hammock nettings, and one aft on the starboard side glanced under her counter, exploding four feet (1.2 m) underwater, damaging her bottom and causing serious leaks.

Richmond joined the West Gulf Blockading Squadron off Ship Island on 5 March as Flag Officer David Farragut prepared to seize New Orleans, Louisiana.

[2] Hidden by intervening woods, the Union mortar flotilla under Commander David D. Porter began a six-day bombardment of the Confederate forts on 18 April 1862.

The Confederates began sending fire rafts downstream, and Richmond reported dodging one in the early morning of 21 April which "passed between us and the Hartford, the great flames shooting as high as the masts."

On 24 April Farragut's fleet ran past the forts, engaged and defeated the Confederate flotilla, and continued upriver for about 12 miles (19 km).

Richmond landed her Marine detachment at New Orleans to help keep order until General Benjamin Franklin Butler's Army troops arrived.

Farragut's fleet again raced past Vicksburg and Richmond continued to provide escort for supply steamers and shore bombardment support.

In one of the fiercest engagements of the war, Farragut's squadron attempted to pass the Confederate fortifications at Port Hudson some 15 miles (24 km) upriver from Baton Rouge on 14 March 1863.

Richmond, lashed alongside USS Genesee, found she could make no headway against the strong current as she came under fire from the shore batteries.

Attempts by General Nathaniel P. Banks' Union Army troops to take Port Hudson on 27 May were no more successful and Federal forces afloat and ashore settled down for a long siege.

Five days later, Richmond and other ships below Port Hudson helped Union ground forces to take possession of that last Confederate bastion on the Mississippi.

Fifteen minutes later as the monitors were preparing to meet the defending Confederate casemate ram Tennessee, USS Tecumseh struck a moored "torpedo" or mine and sank in seconds.

Richmond and Port Royal in turn went hard astern, causing the entire line of wooden ships to fall into disarray.

Arriving at Lisbon on 10 February, she called at various Mediterranean ports during the remainder of the year and during 1870 was stationed at Villefranche and Marseilles to protect U.S. citizens potentially endangered by the Franco-Prussian War.

Departing Norfolk 11 January 1879, Richmond passed into the Mediterranean and through the Suez Canal, hoisting the flag of Rear Admiral Thomas H. Patterson at Yokohama on 4 July 1879.

For four years Richmond cruised among the principal ports of China, Japan, and the Philippines, serving as flagship until 19 December 1883 when Trenton relieved her.

[6] Receiving a new crew at Panama in September 1880, Richmond remained on station until departing Hong Kong for the United States on 9 April 1884.

The following year she steamed to Philadelphia; served there as a receiving ship until 1900; then remained moored at League Island until ordered to Norfolk in 1903.

At Norfolk, she served as an auxiliary to the receiving ship USS Franklin until after the end of World War I. Richmond was struck from the Navy list in June 1919 and sold to Joseph Hyman & Sons, Philadelphia, on 23 July.