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The Dragonfly shares a clear family resemblance with the Dragon Rapide, but is smaller and has higher aspect ratio, slightly sweptback wings. The lower wing has a shorter span than the upper, unlike the DH.89, and the top of the engine nacelles protrude much less above its surface because the fuel tank had been moved to the lower centre section. Structurally, too they are different: the Dragonfly had a new preformed plywood monocoque shell and strengthened fuselage. It was designed as a luxury touring aircraft for four passengers and a pilot, with provision for dual controls. The first aircraft, G-ADNA, first flew on 12 August 1935. The Dragonfly achieved maximum performance on low power, by using the new construction methods developed for the de Havilland Comet racer, and therefore was expensive to buy (£2,650). In modern terms, it was an executive transport, aimed at wealthy private individuals, often via the companies they owned
The first delivery was made in May 1936. Some 36 new-build Dragonflies went to private and company owners, about 15 to airlines/air taxis and three to clubs. Two each went to the Danish and Swedish air forces, and the Royal Canadian Mounted Police had four to combat rum-runners. Production ended in 1938.

By 1939, several aircraft had moved from private to commercial use, like the fleet built up by Air Dispatch Ltd at Croydon Airport, headed by The Hon Mrs Victor Bruce. Amongst her seven examples were also some ex-airline machines. They were used as air taxis between the various London airports, and also as Army Cooperation night flying trainers. Western Airways of Weston-super-Mare Airport used its Dragonfly on a scheduled service via Birmingham to Manchester.

Seven airframes were shipped to Canada, and erected by de Havilland Canada, where they served a variety of small commercial operators, the R.C.M.P. and two with the R.C.A.F. At least one, CF-BFF, was fitted with Edo floats, and used commercially.

In about 1937, three Dragonflies were bought by the Romanian government for crew training, appearing on their civil register

At the start of World War II, about 23 Dragonflies were impressed into the R.A.F and Commonwealth air forces, some six surviving to 1945. Overall, there were about thirteen flying in that year.
Dragonfly used by Silver City Airways as an executive transport in 1953 Silver City Airways operated a Dragonfly G-AEWZ as an executive transport from 1950 until 1960. By around 1970, only the two survivors noted below were active. In May 2018 Hertfordshire-based Uno bus named a fleet of buses after the Dragonfly plane.

The fuel tanks in the Dragonfly are in the thickened lower centre-section, not immediately behind the engines as in the Dragon Rapide. As a result, only one aircraft was lost to fire. A common cause of loss was the frequent development of a vicious ground loop either on takeoff or landing, resulting in undercarriage writeoff and spar damage.