Miles and Straight recognised that they had similar ambitions to develop modern aircraft suited to flying clubs and private owners alike, and thus decided to collaborate on its production.

During late 1935, the Grand Prix motor racing driver, aviator and businessman Whitney Straight was engaged in efforts to establish numerous flying clubs to server major British towns.

[5] As a part of his efforts to popularise aviation, Straight sought a modern aeroplane that would be best suited for both club flying and use by private owners; specifically, he desired the envisioned aircraft to be considerably faster that the slow moving biplanes that traditionally dominated the market.

Miles, the prototype demonstrated the design to already be fulfilling expectations, particularly in regards to its ease of flight and comfort, while also achieving a 50 per cent speed increase over its biplane contemporaries.

[6] Having been sufficiently pleased with the first prototype's early performance, quantity production of the Whitney Straight commenced as soon as possible, a state which was reportedly achieved by April 1936.

[6] The wings of the Whitney Straight were relatively thick for the era; considerable effort had been put into their design to carefully define their drag properties.

[10] The wings were fitted with vacuum-operated split flaps; these were attributed as having enabled the type's relatively low takeoff speed of 50 mph, as well as the aircraft's high rate of climb.

[6] An alternative flap arrangement, that was noticeably more efficient and produced less drag while increasing lift coefficient, was experimented with during the later years of the prototype's flying career; it directly influenced the design of several subsequent aircraft.

[15] Shortly following the outbreak of the Second World War, the Air Ministry impressed 23 Whitney Straights into military service, in which capacity they were operated as communications aircraft.

[9] Between 1939 and 1943, a New Zealand-based aircraft, piloted by Alan Prichard, participated in aerial seed sowing trials at Ninety Mile Beach, and was subsequently used for spreading superphosphate.