The contract to build Churchill was awarded to the Bath Iron Works Corporation on 6 January 1995, and the keel was laid down on 7 May 1998. Churchill was launched 17 April 1999, delivered 13 October 2000, and commissioned 10 March 2001. The launch and christening of the ship was co-sponsored by Lady Soames, the daughter of Sir Winston Churchill and Mrs. Janet Cohen, wife of the United States Secretary of Defense.
USS Winston Churchill is the only active US Navy warship named after a foreign national, and is the first destroyer and only the fourth US warship named after an Englishman. (The others were USS Alfred, an armed merchantman named after King Alfred the Great; USS Raleigh, a continental frigate, named after Sir Walter Raleigh and USS Effingham, named after Thomas Howard the 3rd Earl of Effingham who resigned his commission rather than fight the Americans during the American Revolutionary War.)
On 14 September 2001, (three days after the September 11, 2001 Terrorist Attack), the Deutsche Marine destroyer FGS Lutjens (D-185) passed close aboard Churchill and rendered honors by manning the rails, flying the Stars and Stripes at half-mast, and the display of a banner reading "We Stand By You."