The airport was constructed in the 1950s and was an interceptor aircraft facility for the Soviet Air Force. It initially operated the Sukhoi Su-9 (Fishpot) in the 1960s and 1970s. The regiment replaced it in 1978 with the MiG-23M (Flogger-B). In the 1990s, the Turkmen Air Force took over operation of the military base.

Development since the 2000s

In December 2007, the State National Service Turkmenhowayollary signed a contract with Polimeks to design and build a new airport in Türkmenbaşy. The Turkish company was to reconstruct the existing airport, build a 3.5 km runway, aircraft parking, and a centralized fueling station. Construction began in February 2008.

On April 12, 2010, the new Turkmenbashi International Airport received its first four international flights. The airport features a four-story terminal, a 61-meter control tower equipped by Siemens and Thales, and a VIP facility. It can handle 800 passengers per hour, service 14 aircraft, and accommodate 7 flights at once, meeting international standards.

In 2010, a 22-kilometer motorway was opened, connecting Türkmenbaşy International Airport, located on the Krasnovodsk Peninsula, with Awaza. The Türkmenbaşy International Airport – Awaza motorway is designed for three lanes of traffic in both directions, with a 5-meter-wide median strip. It is equipped with modern road signs, parking bays, and an electronic traffic safety monitoring system. Convenient entrances and exits are provided at junctions, and terrain irregularities are overcome using two-level arched overpasses.

Until 2011, the airfield had the main runway 16/34. The airfield was capable of receiving aircraft of most types, including An-225, An-124 and Il-76 (with partial load), An-22, Tu-154, Boeing-757 and all lighter ones, as well as helicopters of all types. In 2011, the construction of a new runway 16R/34L was completed, its classification number (PCN) is 70/R/A/X/T, dimensions are 3500 × 45 m (cement concrete). The commissioning of the new runway allows the airport to receive aircraft of all types.

Since October 2022, Belavia has been operating regular flights on the Minsk–Türkmenbaşy route.

Starting May 19, 2025, Turkmenistan Airlines temporarily suspends flights connecting Turkmenbashi with Ashgabat, Turkmenabat, Mary, and Dashoguz. Routes redirected to Balkanabat International Airport.

In summer 2025, Turkmenbashi International Airport underwent major modernization in preparation for the 3rd UN Conference on Landlocked Developing Countries in Awaza. Arrival and departure halls were upgraded, passport and customs control points were modernized, and new digital systems were introduced. The airport's technical fleet was expanded with modern equipment, the runway was improved, and services were enhanced to meet international standards. The modernized international airport was put into operation on July 30, 2025. In August 2025, the airport began actively accepting flights, and within a month, regular flights to Ashgabat and Minsk were restored.