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 Home Squadron, 1852
After shakedown out of Norfolk, Powhatan joined the Home Squadron as flagship of Commodore John T. Newton and sailed for New York where she was visited by the Secretary of the Navy, John P. Kennedy. She departed New York on 16 October 1852 for Vera Cruz with the new Minister to Mexico, Judge Alfred Conkling, on board and returned to Norfolk on 27 November via Havana and Pensacola.
 East India Squadron, 1853–1860
Powhatan, under Comdr. William J. McCluney, was next assigned to the East India Squadron and arrived on station via Cape of Good Hope on 15 June 1853. Her arrival in Chinese waters coincided with an important phase of Commodore Matthew C. Perry's negotiations for commercial relations with the Japanese and the opening of two ports. She was Perry's flagship during his November visit to Whampoa. On 14 February 1854 she entered Yedo (Tokyo) Bay with the rest of the squadron and the Convention of Kanagawa was signed on 31 March 1854 (3 March in the old Japanese calendar).
During August 1855 Powhatan accompanied HMS Rattler in a successful battle against Chinese pirates off Kowloon, and reached the U.S. on 14 February 1856 with the new treaty.
The US-Japan Treaty of Amity and Commerce was signed on her deck on 29 July 1858 (19 June in the old Japanese calendar). On 13 February 1860, the Powhatan accompanied by a Japanese capital ship, Kanrin Maru that departed on 9 Feburuary (18 January in the old Japanese calendar), left Yokohama, Japan, en route to San Francisco as part of the first official embassy of the Empire of Japan to the United States of America. The Japanese embassy was formally composed of three men: Ambassador Shinmi Masaoki (新見正興), Vice-Ambassador Muragaki Norimasa (村垣範正), and Observer Oguri Tadamasa (小栗忠順).
 Civil War, 1860–1865
Powhatan remained active throughout the Civil War. She served as Flag Officer Garrett J. Pendergrast's flagship at Vera Cruz during October 1860. In April 1861, while under the command of Lt. David Dixon Porter, she assisted in the relief of Fort Pickens, Florida. President Abraham Lincoln had attempted to countermand the order sending the Powhatan to Fort Pickens and send the ship to assist in the relief expedition to Fort Sumter instead, but because Secretary of State William H. Seward signed the order "Seward" rather than "Lincoln," the order was not obeyed. The Powhatan assisted in the establishment of the blockade of Mobile, Alabama on 26 May, capturing schooner Mary Clinton on 29 May. During July and August Powhatan joined the blockade of the Southwest Pass of the Mississippi River, retaking schooner Abby Bradford on 15 August. From late August to October she pursued CSS Sumter throughout much of the West Indies.
Powhatan operated off Charleston, South Carolina from October 1862 to August 1863, captured schooner Major E. Willis on 19 April and sloop C. Routereau on 16 May, and deployed for a second time to the West Indies from November 1863 to September 1864 as flagship of Rear Admiral James L. Lardner. She participated in the successful reduction of Fort Fisher, 24–25 December 1864 and in its capture on 13–15 January 1865.
 South Pacific Squadron, 1866–1869
After the war, in October 1865, she sailed from Boston with Tuscarora and Vanderbilt, escorting monitor Monadnock to California via Cape Horn. She arrived at San Francisco, California on 22 June 1866.
Powhatan was the flagship of the South Pacific Squadron 1866–1869, commanded by Rear Admiral John A. Dahlgren from 12 December 1866 to 14 July 1868. In March 1866 she was sent to Valparaíso to protect U.S. interests during the Chincha Islands War.
 Home Squadron, 1869–1886
From 1869 to 1886 she was attached to the Home Squadron and was flagship from 15 September 1869 until 30 December 1870 and again from 4 July 1877 until 10 December 1879. During this period, three Powhatan crewman earned the Medal of Honor for rescuing fellow sailors from drowning: Landsman George W. Cutter at Norfolk, Virginia, on 27 May 1872; Seaman Joseph B. Noil at Norfolk on 26 December 1872; and Coxswain William Anderson on 28 June 1878. The ship ended her long and conspicuous career by making numerous cruises in Cuban waters to protect American commerce: July–August 1880, February–May 1882, January–May 1883, January–May 1885, and January–February 1886.
Powhatan was decommissioned on 2 June 1886 and was sold on 30 July 1886 to Burdette Pond of Meriden, Connecticut, and scrapped 5 August 1887.
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