The prototype Venom first took to the air in September 1949, the first FB1 variants entering service with No.11 Squadron in West Germany three years later. The FB4 version arrived in 1955 and introduced a redesigned tail, power-operated ailerons and an ejector seat. The RAF also ordered a two-seat night-fighter version and from this the Sea Venom was developed for the Royal Navy.

The RAF's single-seat Venoms were operated exclusively overseas, equipping the Far East and Middle East Air Forces as well as the 2nd Tactical Air Force in Germany. The last RAF Venoms in use were those of No.28 Squadron in Hong Kong, these being withdrawn in 1962.

Other operators of land-based fighter-bomber Venoms included New Zealand, Iraq, Venezuela and Switzerland. From 1953 a consortium of three Swiss companies built 150 FB1 (including 24 camera-equipped reconnaissance FB1R) and 100 FB4 aircraft for the Swiss Air Force, equipping 11 squadrons by 1965. These were the last Venoms in service, and were finally retired in 1983.

The Vampire was an exceptionally versatile aircraft, and it set many aviation firsts and records, being the first RAF fighter with a top speed of over 500mph. It was the first jet to take off from and land on an aircraft carrier, and in 1948 John Cunningham set a new world altitude record of 59,446 ft (18,119 m). On July 14 1948, Vampire F3s of RAF No 54 Squadron became the first jet aircraft to fly across the Atlantic Ocean. They went via Stornoway, Iceland and Labrador to Montreal on the first leg of a goodwill tour of Canada and the US where they gave several formation aerobatic displays.

The first engine was a Halford H1 producing 2,100 lbf (9.3 kN) of thrust, designed by Frank B Halford and built by de Havilland and later renamed the Goblin. The engine was a centrifugal-flow type, a design soon superseded post-war by the slimmer axial-flow units, and initially gave the aircraft a disappointingly limited range, a common problem with all the early jets. Later marks were distinguished by greatly increased fuel capacities. As designs improved the engine was often upgraded. Later Mk.Is used the Goblin II, the Mk.3 onwards used the Goblin III and the final models used the Goblin III. Certain marks were test-beds for the Rolls-Royce Nene but did not enter production.

The Mk.5 was navalised as the Sea Vampire, the first Royal Navy jet aircraft. The navy had been very impressed with the aircraft since December 3, 1945, when a Vampire carried out the flying trials on the carrier HMS Ocean. The RAF Mk.5 was altered to extend the aircraft's role from a fighter to a ground attack aircraft, the wings being clipped, strengthened and fitted with hard-points for bombs or rockets. The fighter-bomber Mk.5 (FB.5) became the most numerous combat variant with 473 aircraft produced.

The final Vampire was the Mk.11, a trainer. First flown in 1950, over 600 were produced in both air force and naval models. The trainer remained in service with the RAF until 1966.