Tallapoosa remained in service after the war and served in various capacities, including schoolship for midshipmen of the United States Naval Academy.

As Tallapoosa was being fitted out, Confederate cruiser Tallahassee was cruising off the Atlantic coast destroying Union shipping from the Virginia Capes to Nova Scotia.

Her most notable duty during this assignment occurred on 11 January 1865 when she assisted in salvaging material and equipment from screw frigate San Jacinto which had run aground in the Bahamas on an uncharted reef near Green Turtle Cay off Grand Abaco Island.

In January 1870, she carried Admiral David Farragut to Portland, Maine, where he met HMS Monarch at the end of that British turreted battleship's voyage across the Atlantic Ocean to return to the United States the remains of philanthropist George Peabody who had died in England.

Early the following summer, the double-ender carried Farragut from New York City to Portsmouth, New Hampshire, to visit the commandant of the navy yard.

As Tallapoosa neared Portsmouth on 4 July, she fired an Independence Day salute to her famous passenger, the Navy's highest ranking and most respected officer.