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At 6pm on Saturday, Qantas flight QF181 landed its first evening flight to the town, from Sydney.
The plane left at 7.15am yesterday - the resort's first overnight international flight.
Virgin Australia operated its first Queenstown night flight on June 23, while Air New Zealand and Jetstar landed their first after-dark flights last year.
Queenstown Airport chief executive Colin Keel described Saturday's Qantas flight as a ''great moment''.
''It's a shame we couldn't have put on better weather but hopefully those on board will enjoy the new snow it's brought to the skifields,'' he said in a statement.
Qantas and Virgin Australia gained regulatory approval for after-dark flights into Queenstown last month.
Now, all four airlines that fly to the town operate night flights.
Mr Keel: ''It's a huge achievement and the culmination of more than four years of hard work and collaboration by all of the organisations involved who shared a vision and commitment to safety to make after-dark flights a reality.''
Qantas' Sydney-based corporate communication manager Jessica Richards said in a statement higher than expected demand led the airline to add two flights a week on its Sydney to Queenstown route during the July-August ski season peak.
That increased Qantas' flights to and from Queenstown to 10 a week over winter.
Recently, the Australian airline announced it would continue daily direct flights between Sydney and Queenstown year-round.
Mr Keel said evening flights reduced peak-time pressure on the airport's facilities and services during winter, in the face of rising passenger movements and traffic volumes.
In the 12 months to May, total passengers to and from Queenstown were 1.875 million - up 14.9%, or 242,594 passengers, on the year before.
Night flights were also a better use of the airport's consented operating hours of 6am to 10pm, Mr Keel said.
However, they have not been without controversy.
On May 20, a Jetstar flight bound for Melbourne took off at 10.14pm, which breached the airport's resource consent.
After-dark flights for Queenstown were first mooted in 2002.
Transtasman civil aviation regulators signed off the foundation safety case for night flights in May 2014.
Two months later, a senior airline pilot told Mountain Scene he would be ''very uncomfortable'' landing in Queenstown at night.
In November 2015, the New Zealand Air Line Pilots' Association said it had not been properly consulted about the safety case for night flights and it was not happy with safeguards.
Not much has been heard from the association since, however.
Queenstown Airport and Airways New Zealand completed the airport's $19.65 million runway and lighting upgrade in April last year.
In April this year, a $750,000 project to groove the airport's runway was finished.