She is named for American Naval hero, Commodore Thomas Truxtun (1755–1822), one of the first six commanders appointed by George Washington, to the newly formed U.S. Navy.

During construction at Ingalls Shipbuilding, Pascagoula, Mississippi, she suffered a major electrical fire on 20 May 2006, engulfing two levels and causing damage estimated to be worth millions of dollars.

[6] In 2012, the US Navy contracted with L3 Technologies to develop a fuel-efficient hybrid electric drive train for the Flight IIA Arleigh Burke guided missile destroyers.

[7] In March 2018, the US Navy announced that the trial program to install hybrid electric drives in 34 destroyers would be cancelled leaving Truxtun as the only ship so fitted.

The deployment of Truxtun, along with sister ship Donald Cook, to the Black Sea, was intended as a "strategic reassurance" for former Soviet republics and satellite states concerned about the annexation of Crimea by the Russian Federation[9][10] On 10 August 2020, Truxtun completed a deployment with the Dwight D. Eisenhower Carrier Strike Group, without any port calls, that lasted for almost seven months.