The airfield opened in 1940 as a satellite station of RAF Carew Cheriton, primarily to support anti-aircraft co-operation training. Anti-aircraft co-operation units flew slow, brightly painted target aircraft, often Hawker Henleys towing drogues, while ground gunners practised tracking and live firing. Detachments of No. 1, No. 6 and No. 7 Anti-Aircraft Co-operation Units rotated through the field, alongside a brief Polish Army Resettlement Corps depot in 1946 housing soldiers who had fought their way from the eastern front of Europe and now could not safely go home. By December 1943, No. 595 Squadron RAF had formed at Aberporth flying Hurricanes, Tiger Moths, and Ansons in the same target-towing role until the unit disbanded in April 1946. The runways were rough grass strips for much of this period; the brand-new asphalt runway only arrived in 1956, with extensions to the hangar apron through 1968 and 1971.

After the war, Aberporth became a development site for guided weapons. The Royal Aircraft Establishment ran a Ranges Division there from 1939 to 1973; the Bristol Bloodhound Mk.2 surface-to-air missile had a firing unit on site from November 1964 to December 1975. A separate Guided Weapons Range Unit operated from 1958 to 1965, and Joint Services Trials Units tested the BAe Rapier short-range air-defence missile through the early 1970s. Just down the coast, the MoD Aberporth range had begun as a Projectile Development Establishment outstation in 1940 when the threat of German invasion pushed weapons research west from Fort Halstead in Kent. The Clausen Rolling Platform, a strange engineering apparatus that simulates the motion of a ship at sea, was built at Aberporth so that naval radars and missile launchers could be tested without leaving the cliff.

Today the range is managed by QinetiQ, the private company spun out from the old Defence Evaluation and Research Agency in 2001. Air traffic services are provided by NATS from a small tower whose controllers handle some of the most unusual airspace coordination in Europe. The Aberporth Danger Areas extend out over Cardigan Bay and stretch up the coast nearly to Aberystwyth. They can be activated for missile launches, drone trials, or atmospheric research rockets, including civilian scientific launches reaching the lower edge of space. A 2014 BBC article described Aberporth as having a very different kind of air traffic control: not stacking holidaymakers on approach to Heathrow, but choreographing weapons and unmanned aircraft over the open sea.

Since 2006, Aberporth has hosted the West Wales UAV Centre and ParcAberporth, a Welsh Government technology park beside the airfield. The British Army's Thales Watchkeeper WK450 reconnaissance drones, large fixed-wing aircraft with a wingspan of about 11 metres, have been tested here continuously, flying training and surveillance sorties over Cardigan Bay. The work has not been entirely smooth. On 13 June 2018 a Watchkeeper crashed into a lane near the airfield, narrowly missing a primary school sports day in progress nearby; no one was injured but the incident made national news. The Watchkeeper programme was eventually retired in 2024 after a long series of technical difficulties, but the airfield's role as Britain's drone proving ground is settled, and other unmanned platforms continue to fly the bay.

The airport holds a Civil Aviation Authority Ordinary Licence, number P859, which permits flights for the public transport of passengers or for flying instruction. It is not licensed for night use. There is also a small private operation as West Wales Airport, used by light aircraft, although scheduled services have come and gone over the years and the volume is modest. No. 636 Volunteer Gliding Squadron, which gave Air Cadets their first experience of unpowered flight, was based here from October 1996 to December 2001. From the air on a clear day, Aberporth looks like any small coastal airfield: one runway, a handful of hangars, a row of low buildings at the edge of the apron. Watch a little longer, though, and a strange-looking aircraft with no canopy will lift off, climb out to sea, and become a point of light that follows orders without ever hearing a voice.