The railway took over 1,500 workers more than five years to build, with 800 contractors working in the harsh conditions of the Karakum Desert.
The railway was built using no foreign specialists - only companies and contractors from Turkmenistan were used.
The opening ceremony was held at Içoguz (formerly Darvaza), where a white marble railway station with a capacity of 100 people a day was built for the event.
The railway takes 12 hours to traverse, halving the previous travel time between the two cities of Ashgabat and Dashoguz by replacing the route from through Mary and Lebap provinces and along the border with Uzbekistan with one 700 km (435 mi) shorter.
Over 130 bridges span the various water features, and a new highway is also being constructed alongside the railway.