At the outbreak of war, the squadron was called up to full-time service and initially served on defensive duties in the North of England.

During the Battle of Britain, 609 Squadron moved to RAF Middle Wallop as part of Fighter Command's efforts to defend the south coast of England, west of London.

During August 1940 609 Squadron destroyed 46 enemy aircraft, however, by now almost all of the pre war auxiliary pilots were dead or missing.

Almost all of the squadron's original pilots were now lost and replacements came from Belgium, Poland, Canada, Australia, France, United States, and New Zealand in addition to those from Britain.

In November 1941, the squadron was withdrawn from the front line, after 18 months continuous fighting and rested at RAF Digby in Lincolnshire.

It became apparent that the Typhoon was better suited for low level attacks against ground targets, such as airfields and armoured vehicles.

[11] The squadron also gained new pilots, including the first German citizen to fly with the RAF, Film Production Designer Sir Ken Adam.

Prior to the allied invasion of Europe in 1944, 609 Squadron was involved with destroying German radar stations on the French coast.

The Typhoon proved itself adept at the role of 'tankbuster' and went on to attack the German armoured breakthrough at the Falaise Gap in August 1944.

[13] After the war, 609 Squadron was stood down, and the name transferred back to the Royal Auxiliary Air Force.

In 1951, 609 Squadron re-equipped with jet fighter aircraft, the Gloster Meteor, and moved back to Church Fenton in order to take advantage of the longer runway.

The Squadron was deployed to Ali Al Salem as part of Operation Telic from February to August 2003.