The outbreak of the Second World War in Europe in September 1939 saw part of the squadron deployed on coastal anti-submarine and anti-shipping patrols from Madras, before on 1 October 1939, the squadron became a flying training school training pilots for the Indian Air Force, operating de Havilland Tiger Moth and Hawker Hart biplanes as well as Wapitis, and based at Risalpur. Many of the squadron's former operational pilots were employed ferrying Bristol Blenheim bombers from Egypt to India and the Far East, and in January 1941, Blenheims started to be delivered to the squadron, allowing a Blenheim-equipped 27 Squadron to be split off from the training school in February and sent to Singapore. The squadron's Blenheims were Mk IF aircraft, fitted with an under-fuselage gun-pack for use as a long-range and night fighter, and were the only RAF night fighters in the Far East. The squadron moved to Butterworth in May 1941 and to Sungai Petani in August that year. Japan invaded Malaya on 8 December 1941, and 27 Squadron flew off eight Blenheims that morning to attack Japanese invasion shipping. Poor weather prevented them from locating any Japanese ships, however, and air attacks on Sungai Petani that day wrecked the airfield and left the squadron with only four airworthy aircraft. It was evacuated to Butterworth that evening. The remaining aircraft were pulled back to Singapore by 12 December, where they, together with a few Blenheim Is from other squadrons operated under the name of 27 Squadron. The remaining Blenheims based at Singapore, including those of 27 Squadron were evacuated to Sumatra from 23 January 1941, ending up operating from Palembang. On 14 February four of its Blenheims attacked Japanese ships invading Sumatra, with the loss of two Blenheims, with all airworthy aircraft evacuating to Java on 15 February. Here the squadron effectively ceased to exist.