During World War II, she served as a convoy escort in the battle of the Atlantic, sinking one German submarine by ramming, on anti-submarine patrols during the invasion of Normandy, and was employed as a troop transport after VE Day for returning Canadian servicemen, before being decommissioned in mid-1945.

Kempenfelt carried a maximum of 473 long tons (481 t) of fuel oil that gave her a range of 5,500 nautical miles (10,200 km; 6,300 mi) at 15 knots (28 km/h; 17 mph).

A Type 286 short-range surface search radar was also added as was an HF/DF radio direction finder on a short mainmast.

[6] Built as a flotilla leader, she displaced 15 long tons more than the rest of her class and carried an extra 30 personnel.

[10] Kempenfelt was purchased before the war began by the Canadian government, but it agreed to allow the British to retain her until the Royal Navy could compensate for her loss by requisitioning enough auxiliary anti-submarine vessels.

The ship was not fitted with the steam heating necessary to operate in a Canadian winter and she was transferred to the Caribbean in exchange for the destroyer HMCS Saguenay.

[12] Assigned to the North America and West Indies Station, the highlight of the ship's service in the Caribbean was the capture of the German blockade runner MV Hannover in the Mona Passage between the islands of Hispaniola and Puerto Rico on the night of 8/9 March 1940.

Initially intercepted by the light cruiser Dunedin, the crew of Hannover disabled their steering gear and set the ship on fire.

The two ships swapped roles in the morning and the destroyer put some of her crew aboard Hannover to help Dunedin's boarding party fight the fire while the cruiser towed the freighter to Kingston.

[10] In early August, Assiniboine, her sister Restigouche and the ex-American destroyer HMS Ripley, escorted the battleship Prince of Wales to Placentia Bay where Prime Minister Winston Churchill met President Franklin Roosevelt for the first time.

It also claimed the only Canadian casualty during the engagement: Ordinary Seaman Kenneth "Wiley" Watson from Revelestoke, British Columbia.

This caused Lieutenant Sorber, the senior surviving officer, to order the submarine to dive, but this meant that she had to hold a straight course while doing so.

[15] A number of survivors were rescued by Assiniboine and the British corvette Dianthus, before the former ship departed for home for repairs as she was taking on water below the waterline.

[10][16] Whilst en route to Londonderry, Assiniboine dropped a shallow pattern of depth charges on a submarine contact and badly damaged her stern on 2 March 1943.

[17] She remained in British waters for the rest of the war; the ship was damaged in a collision with SS Empire Bond on 14 February 1945 and was under repair until early March.

[10] Assiniboine returned to Canada in June and was briefly used as a troop transport before a boiler room fire on 4 July effectively ended her career.