No. 610 Squadron was formed at Hooton Park on 10 February 1936 as a day bomber unit of the Auxiliary Air Force. Initially equipped with Harts, it began flying training in May 1936 and in May 1938 re-equipped with Hinds.
On 1 January 1939, the squadron was redesignated a fighter unit but retained its Hinds in anticipation of the arrival of Defiants. On the outbreak of war it received Hurricanes, but by the end of September 1939 had exchanged these for Spitfires, becoming operational on 21 October.
When the German offensive opened in May 1940, No 610 moved to Biggin Hill and helped to provide fighter cover for the Dunkirk evacuation beaches and shipping. After taking part in the Battle of Britain, the squadron was moved north to rest and re-equip, returning south in December to go on the offensive.
After nine months of sweeps and patrols, the squadron returned to Yorkshire for eight months in August 1941, moving to East Anglia in April 1942 for shipping reconnaissance missions. In October 1942 it moved to the north of Scotland, returning south in January 1943. In July 1944, No.610 took its Spitfire XIVs to south-east England to intercept flying bombs for two months. In December the squadron moved to the Continent to join No.127 Wing for sweeps over Germany.
It returned to the UK in February 1945 and disbanded on 3 March 1945.