Truculent spent much of her World War II wartime service in the Pacific Far East, except for a period in early 1943, operating in home waters. Here she sank the Nazi German U-Boat submarine U-308, on her first war patrol, with all hands. She also took part in Operation Source, towing X-class midget submarines in an attempt to neutralise the heavy German Navy warships Tirpitz, Scharnhorst and Lutzow.
On transfer to the Pacific, she sank the Japanese army cargo ship Yasushima Maru, the small Japanese vessel Mantai, the Japanese merchant cargo ship Harugiku Maru and five Japanese sailing vessels. She also laid mines, one of which damaged the Japanese minelayer Hatsutaka.
She survived the war and returned to the UK to continue in service with the Navy.
On 12 January 1950 Truculent was returning to Sheerness, having completed trials after a refit at Chatham. In addition to her normal complement she was carrying an additional 18 dockyard workers. She was travelling through the Thames Estuary at night. At 7 o’clock a ship showing three lights appeared ahead in the channel. It was decided that the ship must be stationary and as Truculent could not pass to the starboard side without running aground, the order was given to turn to port. At once the situation became clear as the Swedish oil tanker Divina, on passage from Purfleet and bound for Ipswich, came out of the darkness: the extra light indicated that she was carrying explosive material. A collision was unavoidable. The two vessels remained locked together for a few seconds before the submarine sank.
57 of her crew were swept away in the current after a premature escape attempt, 15 survivors were picked up by a boat from the Divina and five by the Dutch ship Almdijk. Most of the crew survived the initial collision and managed to escape, but then perished in the freezing cold mid-winter conditions on the mud islands that litter the Thames Estuary. 64 people died as a result of the collision. Truculent was salvaged on 14 March 1950 and beached at Cheney Spit. The wreck was moved inshore the following day where ten bodies were recovered. She was refloated on 23 March 1950 and towed into Sheerness Dockyard. An inquiry attributed 75% of the blame to Truculent and 25% to Divina.
Her loss led Peter de Neumann of the Port of London Authority to develop plans for a port control system, and the later introduction of the 'Truculent light', an extra steaming all round white light on the bow, on British submarines, to ensure they remained highly visible to other ships.
On 21 February 1950 the film "Morning Departure" was released. The film tells the story of a British submarine that sinks on a training cruise from the perspective of a small group of survivors. Filming finished shortly before HMS Truculent sank, and the film was almost withdrawn. The decision was made to release the film as planned, and to add the following message that appears in the opening credits of the film.
This film was completed before the tragic loss of HMS Truculent, and earnest consideration has been given as to the desirability of presenting it so soon after this grievous disaster. The Producers have decided to offer the film in the spirit in which it was made, as a tribute to the officers and men of H.M. Submarines, and to the Royal Navy of which they are a part.