USS Powhatan found herself at Vera Cruz, Mexico when war broke out between the states back home. She was recalled home and expected to partake in the relief of besieged Federal forces at Fort Sumter, South Carolina. Instead, she was reassigned to Fort Pickens, Pensacola, Florida which reduced the available guns available to the Fort Sumter situation (while Florida siding with the South, Fort Pickens remained under the control of Federal forces).
Powhatan arrived offshore of Fort Pickens on April 20th with the intent to challenge the Confederate harbor defenses. However, the mission once again changed and Powhatan was relegated to police nearby waters for Confederate activity. With the situation at the fort contained, Powhatan was ordered as part of the force blockading Mobile, Alabama and the Mississippi River on May 26th. She managed the capture of a pair of schooners (Mary Clinton and Abby Bradford) during a period from May to August and chased the CSS Sumter throughout the West Indies into October (though this latter action without success).
From October 1862 until August 1863, Powhatan found herself in waters off of Charleston, South Carolina where she captured another enemy schooner (Major E. Willis) a sloop (C. Routereau) in two separate actions. From November 1863 to September 1864, she served as Flagship to Rear Admiral James L. Lardner before engaging the enemy at Fort Fisher in North Carolina (the Battle of Fort Fisher, December 23-27, 1864). The fort fell in January of the following year.
The American Civil War officially ended (by declaration) on May 9th, 1865 leaving Powhatan as a survivor of the long-running bloody conflict. In October of 1865, she departed Boston waters and ended at San Francisco before being made flagship of the South Pacific Squadron in 1866. She served in this charge until 1869. Powhatan was returned to the Home Squadron as its flagship and served in this position until December 1870. She managed several Caribbean cruises before being formally decommissioned on June 2nd, 1886. Her hulk was sold off for scrap shortly thereafter.
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