In 1952, Cessna initiated the design of a new five/six-seat twin-engined light monoplane designated Cessna Model 310. The prototype flew for the first time on 3 January 1953, proving in production form to be a popular twin. Of low-wing configuration and with tricycle landing gear, the prototype was powered by the 168kW Continental O-470, an engine developed originally for military use under the designation E225. Its use to power the Cessna Model 310 was one of its first civil applications, early production aircraft having the more powerful 194kW IO-470. Good identification features of the design at that time were the two wingtip fuel tanks, then representing the entire fuel tankage.

Production deliveries began in 1954, with steady product improvement continuing year by year. A de luxe version with turbocharged engines, air-conditioning and an oxygen system as standard was introduced in 1966. This was then named the Turbo-System Executive Skyknight being known also for a short period as the Model 320, but later marketed as the Turbo T310. Final versions were the basic Model 310 with 213kW Continental IO-520-MB engines, the structurally identical Model 310II which incorporated a factory installed avionics/equipment package, the Turbo T310 with TSIO-520-BB powerplants and the Turbo T310 II with the same additional equipment fit as the Model 310 II. In the mid-1950s, following competitive selection, a slightly modified version of the Model 310 was ordered for light cargo-liaison duties with the US Air Force under the designation L-27A, subsequently redesignated U-3A A total of 160 were built followed by 36 U-3Bs equipped for all-weather operation, and all were nicknamed 'Blue Canoes'. When production finished in 1981, 5,241 commercial examples of the Model 310 had been built, including a small number for the French air force, plus the 196 delivered to the USAF.

In December 1971 Cessna announced the introduction of the pressurised Model 340 developed from the Model 310. Powered by twin TSIO-520-NB engines each giving 213kW, the 340 incorporated the wing and tricycle landing gear developed for the Model 414, married to a new pressurised fuselage, but using the tail of the Model 310. This was followed in the mid-1970s by the Model 340A equipped with 231kW engines and later by the similarly powered Model 340A II fitted with comprehensive factory-installed avionics allowing IFR operation. In 1978 Cessna introduced the Model 340A III equipped with an improved avionics package including colour weather radar and this version remained available until 1985 when the type was taken out of production, by which time 1,287 had been delivered.

A lightweight unpressurised version of the Model 340 was off ered to the market in 1979 as the Model 335, later available as the improved Model 335 II version, but production ended in 1980 after only 45 had been built.