The $2.3 bn (£1.8bn) airport is located in Ashgabat, the capital, and has the capacity to process more than 1,600 passengers an hour.
But few foreigners visit the isolated Central Asian country, known for its autocratic leadership and vast energy reserves.
Just 105,000 tourists visited in 2015, government figures show, and it is difficult to get a visa.
President Gurbanguly Berdymukhamedov touted his country`s "solid transit potential".
Ashgabat boasts several other unique structures, including a publishing house in shape of an open book.
The city also has two giant golden statues of both Mr Berdymukhamedov and his late predecessor Saparmyrat Niyazov.
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