They were to combine the heavy anti-aircraft armament of the Bittern-class sloops (i.e. six 4 inch (102 mm) QF Mk XVI dual purpose (anti-ship and anti-aircraft) guns in three twin mounts) with a speed of 29 knots (54 km/h; 33 mph) (compared with 18+3⁄4 knots (35 km/h; 22 mph) for the Bitterns) to allow them to work with the fleet when necessary.

[2] An inclining test when the ship was fitting out showed that she, and by extension all the Hunts, was dangerously unstable owing to a design error.

[a] To restore stability to acceptable levels, one twin 4 inch mount was removed, the ship's superstructure and funnel was cut down and additional ballast was fitted.

[1] Following commissioning and initial trials, Atherstone joined the First Destroyer Flotilla based at Portsmouth employed on convoy escort duties in the English Channel.

[13] On 11 September 1940, while escorting Convoy CW11 in the Channel, Atherstone was hit by two bombs and near missed by a third, sustaining serious damage and killing 5 men.

[12][13][14] After repair at Chatham Dockyard, the ship rejoined the First Destroyer Flotilla in January 1941, resuming convoy escort duty in the Channel.

Atherstone and her sister ship Tynedale escorted Campbeltown and the remainder of the strike force, towing the Motor Gun Boat MGB 314 on the passage to St Nazaire.

[18][19] On 26 November 1943 she rescued about 70 survivors from the troopship HMT Rohna, which had been sunk by a Henschel Hs 293 glide bomb off the coast of French Algeria.

On 23 November 1957, Atherstone was transferred to the British Iron & Steel Corporation for disposal, and was towed to Port Glasgow for scrapping by Smith & Houston.