On commissioning, Jaguar joined the 7th Destroyer Flotilla based at Grimsby, operating off Britain's east coast.

She was refitted at the Caledon Shipbuilding & Engineering Company's Dundee yard from 15 March 1940 to 1 May that year, with leaks being rectified and her fuel tanks modified.

[5] On 20 May 1940, Jaguar, along with sister ships Jackal and Javelin and the corvette Puffin, escorted Naval trawlers as they cut the undersea telegraph cables between the UK and Borkum.

[6][7] On 26 May 1940, the Royal Navy set Operation Dynamo in motion, to rescue trapped British troops from Dunkirk and the surrounding area.

She embarked about 1000 troops before leaving the harbour at about 15:50 hr, when she was attacked by dive bombers and near missed by four bombs, which severed a steam pipe, which disabled her engines and knocking out her steering.

Jaguar was covering the evacuation when she encountered the Italian destroyer Francesco Crispi in the early hours of 27 February.

After a brief exchange of fire between the two ships, Jaguar's searchlight was hit by a 40 mm (1.6 in) round from Crispi, causing contact to be lost.

[19] On the night of 20/21 April 1941, Jaguar formed part of the escort for the battleships Warspite, Valiant and Barham and the cruiser Gloucester when they bombarded the port of Tripoli in Libya.

[19][23] On 23 April, Jaguar together with sister ships Janus, Jervis and Juno set out from Malta to intercept an Italian convoy on the way from Italy to Tripoli.

On 1 December 1941, her bridge was hit by a single 4.7 in shell accidentally fired by Jervis while the latter destroyer guns were being cleaned.

[19] Later that month, Jaguar was deployed to Malta for operations against Italian convoys carrying supplies to North Africa.

Jaguar broke into three parts and quickly sank off Sidi Barrani, Egypt, 31°53′N 26°18′E / 31.883°N 26.300°E / 31.883; 26.300 with the loss of 3 officers and 190 of her crew, including two from the Irish Republic which was neutral at the time.