Sailing from Norfolk 23 January 1945 to escort Bon Homme Richard (CV-31) to Trinidad, Drexler then sailed on to reach San Diego 10 February. Three days later she got underway for Pearl Harbor for antiaircraft and shore bombardment exercises until the 23d when she sailed on escort duty to Guadalcanal and Ulithi, the staging area for the Okinawa invasion.

Drexler departed Ulithi 27 March 1945 bound for Okinawa and dangerous duty on a radar picket station. On 28 May at 0700 two suicide planes attacked Drexler and Lowry (DD 770). The first was downed by the combined fire of the two destroyers and planes from the combat air patrol. The second tried to crash Lowry and failing, stumbled into Drexler, cutting off all power and starting large gasoline fires. Despite the heavy damage she kept firing, joining in splashing three planes which attacked immediately after the crash. At 0703 yet another suicider crashed in flames into Drexler’s superstructure. A tremendous explosion followed and the destroyer rolled on her starboard side and sank stern first in 27°06' N., 127°38' E., less than a minute after the second hit. Because of the speed with which she sank, casualties were heavy: 158 dead and 52 wounded, including the commanding officer.

Drexler received one battle star for World War II service.