The airport was built in the late 1930s to provide air services to a number of Scottish airports. From 1940 it was an RAF fighter base to intercept Luftwaffe raids from Norwegian bases, protect the Shetlands but also as reserve cover for the Home Fleets northern anchorage at Scapa Flow, further south in the Orkney Isles. Sumburgh became Shetlands premier airport over Lerwick (Tingwall) in 1953 and because of its proximity to the mainland. In 1971, in response to the North Sea hydrocarbon exploration and production industry, a brace of C-47s began scheduled services from Aberdeen and helicopter operations soon followed.
Its perimeter road curves around three-quarters of the airfield to the main terminal, built in 1979. Since 1982 the Wilsness Terminal has supplemented passenger movements. To improve reliabilty, a PAMOS weather monitoring system was installed in 1997 but in December 1999, the majority of North Sea oil-related helicopter operations transferred further north to Scatsta, nearer the Sullom Voe oil terminal. It also moved the traffic away from the conspicuous Sumburgh Lighthouse (an 1821 marvel from the prolific Stephenson family, for the Northern Lighthouse Board) and the important Old Scatness Broch archaeological site. Sumburgh is the most northerly SAR base, towards the northern margin of the UK Search and Rescue Region