With the onset of the American Civil War in April 1861, Colhoun returned to U.S. Navy service, becoming an acting lieutenant on 24 September 1861. From 1861 to 1862 he was commanding officer first of the steam tugboat , then of the steamer , both operating as part of the Union blockade of the Confederate States of America in the North Atlantic Blockading Squadron. In command of "Hunchback", he saw combat at the Battle of Roanoke Island on 7–8 February 1862, the Battle of New Bern on 14 March 1862, and in an engagement on the Blackwater River south of Franklin, Virginia, on 3 October 1862 during the joint expedition against Franklin.