Ottawa joined the South Atlantic Blockading Squadron for service in the waters of the Carolinas, Georgia, and Florida. During the Civil War she participated in nineteen operations against ships and shore installations from Hilton Head, South Carolina, to the St. Johns River in Florida.
These included capture of Fort Walker and Fort Beauregard, Port Royal Sound, South Carolina, 7 November; covering the landing of U.S. troops at Wassaw Sound, Georgia, 26 January 1862; capture of Fernandina, Florida, 4 March; attacks on Fort Wagner, Charleston Harbor, South Carolina, from 18 July 1863 to 18 August and on the Confederate batteries on Morris Island from 31 July to 20 August.
Ottawa also assisted the U.S. Army in the occupation of Bull's Bay, South Carolina, 11 February 1865. Other engagements took place with the batteries at Brown's Landing, St. Johns River, Florida, and at Palatka, Florida.
Ottawa returned north and was decommissioned on 12 August 1865 at the New York Navy Yard where she was sold at auction on 25 October for $13,200.