Ajax served on the America and West Indies Station from completion, then part of South American Division on the outbreak of the Second World War in September 1939. Operating off the River Plate, she intercepted the German merchantmen Carl Fritzen, Olinda, and Ussukuma. As part of Force G she participated in the hunt for, and action with, Admiral Graf Spee, being hit seven times during the Battle of the River Plate, 13 December 1939, when she was the flagship of Commodore Henry Harwood.
Under repair until July 1940, she then moved to the Mediterranean. On 11/12 October 1940 she engaged Italian forces, sinking the torpedo boats Airone[?] and Ariel, and badly damaging the destroyer Artigliere[?], which was later sunk. Ajax participated in the Battle of Cape Matapan and the evacuation from Crete, removing the last troops on 29 April 1941. She was hit by bombs from Ju87's on 21 May, covered Syrian operations in June, and joined Force K at Malta in November 1941, but was withdrawn February 1942.
She was refitted in England, May-October 1942, then returned to Mediterranean where she was damaged by bombs again, necessitating repairs in New York between March and October 1943. Ajax returned to Mediterranean again, then to Normandy with Force K at Gold Beach for the D-Day landings, and at landings in S. France. Ajax operated in Aegean during reoccupation of Athens and the communist uprising in Greece.
Laid up postwar, she was broken up in November 1949.
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