HMS Jaguar (F 34) took part in Operation Dynamo, the evacuation of Dunkirk. On 28 May, the destroyer brought 700 troops to Dover and was returning the next day to pick up more, when she was attacked at 11.55 hours by 17 German Ju87 dive-bombers. One of them was damaged by her AA fire and later shot down by a fighter. She was attacked again at 15.00 hours and badly damaged by a near miss. The engines and steering were put out of action and a hole was opened near the waterline. The destroyer was taken in tow until the engines were repaired and she reached Dover under own power. One DSC, two DSM and twelve MiD were awarded to crew members from this ship for this action.
After repairs the vessel continued to operate in Home Waters until November, when she left the Clyde for Gibraltar as escort for HMS Renown (72) to join the Force H at Gibraltar.

On 11 October, HMS Jaguar (F 34) took part in Operation Medium, the shelling of Cherbourg by HMS Revenge (06), together with the destroyers of the 5th Flotilla and MTBs. On 27 November, the ship was in action with the Italian Fleet off Cape Spartivento.

Early in January 1941, the destroyer took part in Operation MC4, the covering of a convoy from Gibraltar to the Eastern Mediterranean and arrived Malta on 10 January, escorting HMS Illustrious (87), which had been badly damaged by bombs. Later that month, she also took part in Operation Ration, the interception of Vichy French ships.

During the night 27/28 February, the destroyer covered the landing of troops at Castelorizo, in the Dodecanese, and during the withdrawal had a slight engagement with the Italian destroyer Crispi. On 3 April, HMS Jaguar (F 34) and HMS Janus (F 53) were ordered to Port Said to intercept four Italian destroyers, which had been reported heading northward off Port Sudan. However, these destroyers were deterred by aircraft from HMS Eagle (94). In May 1941, the destroyer took part in the Battle for Crete and was one of the few ships which escaped damage. The ship then served one month with the Force H during the Syrian campaign. In July, the ship took part in Operation Guillotine, to bring RAF personnel to Cyprus from Port Said. The ship operated the next few months off the Lybian coast, bombarding the Bardia area in October.

On 20 December, HMS Jaguar (F 34) (LtCdr L.R.K. Tyrwhitt, DSC, RN) picked up eight officers and 17 ratings from HMS Kandahar (F 28), which had struck a mine off Tripoli and finished off the badly damaged destroyer by a coup de grâce. The destroyer was then assigned to the 14th Destroyer Flotilla and carried out escort duties in the Mediterranean during the first three months of 1942. On 18 January, she had been part of Force K, which escorted a convoy from Alexandria to Malta and back.

At 02.27 hours on 26 March 1942 HMS Jaguar (F 34) (LtCdr L.R.K. Tyrwhitt, DSO, DSC, RN) was attacked by U-652 with a spread of four torpedoes northest of Sidi Barrani, Egypt. Two of the torpedoes struck forward, set the ship on fire and caused her to sink in a short time. The commander, two officers and 190 ratings were lost. Eight officers and 45 ratings were picked up by HMS Klo (Lt. English, RNR) and taken to Mersa Matruh.

The destroyer had been part of the escort for the fleet oiler Slavol, which was sunk two hours later by the same U-boat.