During the American Civil War, he won distinction for his service in the Mississippi Squadron at the Battle of Fort Henry on 6 February 1862; and at Pittsburgh Landing on 1 March 1862; and again on 6 and 7 April 1862.

On 1 July, the Battle Fleet sailed on a goodwill cruise to the Southwest Pacific, and Shirk visited Melbourne; Lyttelton and Wellington; and American Samoa before returning to San Diego on 26 September.

She was overhauled at Mare Island from 11 January to 26 February 1926 and operated out of San Diego until departing on 14 June for summer exercises off Washington.

On 7 February 1927, Shirk sailed from San Diego and participated in exercises off Panama and, after transiting the Canal on 5 March, operated in the Caribbean with the fleet.

She departed the Caribbean on 22 April and visited New York, and conducted a joint Army and Navy exercise in Narragansett Bay before arriving at Hampton Roads on 29 May 1927 for the Presidential review.

She arrived in the Panama Canal Zone on 9 June 1927 for duty off Nicaragua with the Special Service Squadron, protecting lives and property of American and other foreign nationals there supporting peacekeeping operations.

Shirk was struck from the Navy list on 22 July 1930, scrapped at Mare Island, and her hulk sold there on 27 January 1931 to P. J. Willett.