Zaha Hadid Architects' stadium is one of several new venues being built for the football tournament in 2022, and is first to complete.
In total, eight venues will be used during the World Cup, including the Khalifa International Stadium that was redeveloped in 2017 and the 80,000-seater Lusail Stadium designed by Foster + Partners.
Another of the venues, the Ras Abu Aboud Stadium, will be built using shipping containers.
The distinctive form of Zaha Hadid Architects' Al Wakrah Stadium was taken from the shape of the typical fishing boats – called dhows – that can be seen in the city's harbour.
However, when visualisations of the stadium were first revealed many people compared its shape to female genitalia.
The stadium has a fully retractable roof so that the players and spectators can be cooled, allowing for the building to be used all-year round.
"I am certain that in 2022 Al Wakrah Stadium will be one of the most iconic venues at the World Cup, and it gives us all a sense of great pride to be opening the second Qatar 2022 stadium with three and a half years to go," said Jassim Al Jassim, head of venues operations at the Supreme Committee for Delivery & Legacy.
"I look forward to working together with all our stakeholders, friends and colleagues over the coming years to enjoy many more momentous occasions."
Following the World Cup, the capacity of the stadium will be reduced to 20,000 in a similar manner to the studio's London Aquatic Centre, which had its capacity reduced form 17,500 to 2,800 following the 2012 Olympic Games.
The stadium will also become the permanent home of football team Al Wakrah Sports Club.
Photography is courtesy of the Supreme Committee for Delivery & Legacy unless stated.