249 Squadron was formed on 18 August 1918 at Dundee as a seaplane squadron flying anti-submarine patrols along the east coast of Scotland. The Squadron was disbanded on 8 October 1919.

On 16 May 1940 the Squadron was reformed at RAF Church Fenton. Initially equipped with Spitfires, a month later the Squadron was re-equipped with Hurricanes. The Squadron was based at Boscombe Down during the initial part of the Battle of Britain, but in September 1940 it was moved forward to North Weald. Following the end of the Battle of Britain the Squadron went on to serve in Malta in 1941 and Italy in 1943. After the war the Squadron served in the Middle East during the Suez crisis. It was disbanded on 24 February 1969.