The Australian city was named the preferred bidder before being proposed by the IOC executive board in June.
It will be the third time the country has hosted the Olympics after Melbourne in 1956 and Sydney in 2000.
“It’s a historic day not just for Brisbane and Queensland, but for the entire country,” said Prime Minister Scott Morrison.
“Only cities around the globe can host the Olympic Games. This is a fitting recognition of Brisbane’s position in our region and across the world. “
The announcement was greeted by cheers from the Brisbane delegates at the IOC session in Tokyo while fireworks were set off in the Australian city, where people had gathered to await the vote.
“The International Olympic Committee has the honor to announce that the Games of the 35th Olympiad are awarded to Brisbane, Australia,” said IOC president Thomas Bach.
The state of Queensland hosted the 2018 Commonwealth Games and the Brisbane bid was praised for its high percentage of existing venues, a good masterplan, experience in organizing major events, and favorable weather.
The plans made use of 84% existing or temporary venues, with the Gabba cricket ground set to be rebuilt to become the lead venue.
The IOC changed its bidding rules in 2019 to reduce costs and make the process easier for cities.
Several cities and countries had expressed an interest in hosting the Games, including Indonesia, China, Doha in Qatar, Budapest in Hungary, and Germany’s Ruhr region.
Brisbane’s victory looked a certainty after it was unanimously selected as the single candidate for 2032 by the IOC’s 15-strong executive board.
“The Olympic Games in Brisbane will be in the most diligent, grateful, and enthusiastic hands,” said Australian Olympic Committee chief John Coates, who is an IOC vice-president.
The decision means the IOC has now secured hosts for the next three Summer Games with Paris in France staging the 2024 Games and Los Angeles in the United States to host the 2028 Olympics and Paralympics.