[10] The outbreak of war saw Sharpshooter clearing channels through minefields around Scapa Flow and off Loch Ewe and the Clyde estuary.

Sharpshooter's bow was badly damaged, and she was towed back to Dover by the tugboat Foremost 22, the journey taking 11 hours.

[15] She was under repair at Sheerness dockyard and Leith until September 1940, the opportunity being taken to fit Sharpshooter with equipment for sweeping magnetic mines.

[6][14] On 20 February 1941 Sharpshooter was approaching Harwich with sister ships Bramble, Britomart, Seagull and Speedy when they came under attack by two German aircraft.

[6][17] On 27 November 1941 she set out from Hvalfjord in Iceland as part of the escort of the Arctic convoy PQ 5 to Archangel in the Soviet Union.

[18] Sharpshooter remained in Russia, minesweeping and providing local escort for Arctic convoys as they arrived and left Russian ports.

[20] At about 8.25 pm on the evening of 24 March 1942[21] while escorting QP 9 [22] the leading gunner on the forward four-inch gun of Sharpshooter spotted German submarine U-655 on the surface beam on, about two to three cables (370 to 556 meters) away and about 10 degrees off the minesweeper's starboard bow, with no crew apparently manning the conning tower or deck.

[23] The submarine turned rolled over due to the impact and bumped along the minesweeper's port side sinking as it disappeared astern and sank stern first south-east of Bear Island, in approximate position 73.00N, 21.00E.

After shoring up the forward mess deck, she continued at slow speed to Iceland independent of the convoy, and from there to Leith for repair.

[28][6][20] In April 1943 Sharpshooter was ordered to join the 12th Minesweeping Squadron in the Mediterranean, and in July the year took part in Operation Husky, the Allied invasion of Sicily.

[6][29] After Husky, Sharpshooter continued to carry out minesweeping and convoy escort operations in the Mediterranean until October 1944 when she returned to home waters.

[33] On 13 October 1947 she collided with the merchant ship MV Celebes and after repair continued survey duties before returning to Britain at the start of 1948.

A large scale salvage effort was launched by the Royal Navy to locate and recover the wreckage, so the cause of the accident could be determined.