Berdymukhamedov said the new airport's two passenger terminals would have the capacity to serve 17 million passengers a year while the freight terminal could handle 200,000 tons of freight annually.
The five-floor airport is built in the shape of a giant bird -- echoing the logo of the Central Asian state carrier Turkmenistan airlines -- by Turkish construction company Polimeks who won a $2 billion contract in 2013.
A source at the carrier told AFP on condition of anonymity that the new airport cost $2.35 billion by the time it was completed.
Turkmenistan welcomed 105,000 tourists in 2015 according to the state tourism committee, but makes efforts to boost the sector despite a restrictive visa regime.
"With an advantageous geographical position at the crossroads of regional and international communications routes, our country has a solid transit potential we aspire to realise to the maximum," said Berdymukhamedov, 59, at the airport opening.
Turkmenistan has fallen on difficult economic times after the collapse in global prices for hydrocarbons, which make up nearly all the country's exports.
Despite Berdymukhamedov officially encouraging belt-tightening, the country has continued to spend heavily on infrastructure ahead of the 2017 Asian Indoor and Martial Arts Games it will host in Ashgabat.
The existing airport near the capital mainly caters to the state carrier and a short list of foreign airlines from Belarus, China, Russia and Turkey.
The country on Wednesday passed constitutional changes that will effectively allow Berdymukhamedov to rule for life, in the tradition of other strongmen in the ex-Soviet region.
Ashgabat, a white marble-clad city of one million people hosts golden statues of both Berdymukhamedov and erratic late predecessor Saparmurat Niyazov, whose own effigy rotated with the movements of the sun.
