By the early 1960s, Soviet international and internal trunk routes were served by Aeroflot, the state airline, using jet or turboprop powered airliners, but their local services, many of which operated from grass airfields, were served by obsolete piston-engine aircraft such as the Ilyushin Il-12, Il-14 and Lisunov Li-2. Aeroflot wanted to replace these elderly airliners with a turbine-powered aircraft, with the Yakovlev design bureau being assigned to design it. High speed was not required, but it would have to be able to operate safely and reliably out of poorly equipped airports with short (less than 700 m or 2,300 ft) unpaved runways in poor weather.

Yakovlev studied both turboprop and jet-powered designs to meet the requirement, including Vertical Take-Off and Landing designs with lift jets in the fuselage or in wing-mounted pods, but eventually they settled on a straight-winged tri-jet carrying 20 to 25 passengers. The engines were to be the new AI-25 turbofan being developed by Ivchenko at Zaporozhye in Ukraine.

The Yak-40 was the first Soviet-built airliner designed to Western airworthiness requirements.

Aircraft of similar role, configuration and era are: Fokker F28, Fokker 70, VFW-Fokker 614.