The World Cup finals will be expanded to 48 teams from the 2026 edition, football governing body FIFA confirmed at a council meeting in Zurich on Tuesday.
The proposal was backed "unanimously" according to FIFA on Twitter and represents a 50 per cent increase from the present number of 32 teams.
It was the favoured plan of FIFA president Gianni Infantino, who pledged to increase the size of the tournament during his election campaign.
Speaking in a post-meeting news conference, Infantino said that the move was to "shape the World Cup of the 21st century."
Participating countries will be divided into 16 groups of three at the finals, likely creating a tournament with 80 matches - up from the current 64.
Penalty shoot-outs could also be used following draws in group matches in a bid to make it collusion between teams harder.
"There are a various models that could be decided upon," Infantino said.
The top two in each group would progress to the knock-out stage which would begin with 32 teams - meaning the eventual winners lift the trophy after seven matches, as they do now, something Infantino was at pains to stress.
The allocation of finals spots is likely to be decided at the FIFA congress in May and will be hotly contested. Infantino has already promised more places to Africa and Asia, who had only five and four teams respectively at the 2014 edition.
"Football is more than just Europe and South America, football is global," Infantino said.
European countries currently dominate the tournament and regional body UEFA is expected to ask for an increase from 13 to 16 spots from 2026, giving it a third of the places.
But the proposal to increase the size of the competition has not been universally welcomed across the sport with the European Clubs Association (ECA) a particular opponent.
"We fail to see the merits to changing the current format of 32 that has proven to be the perfect formula from all perspectives," the ECA said in a statement Tuesday.
"Questionable is also the urgency in reaching such an important decision, with nine years to go until it becomes applicable, without the proper involvement of stakeholders who will be impacted by this change.
"We understand that this decision has been taken based on political reasons rather than sporting ones and under considerable political pressure, something ECA believes is regrettable."
Reigning World Cup champions Germany expressed disappointment at the decision and questioned the sporting merit of bringing more nations to the finals.
"I still find the current World Cup format with 32 teams good and, from a sporting view, that nothing can be gained from an increase," coach Joachim Loew said on the German federation DFB website.
DFB president Reinhard Grindel said he was "not happy" with the decision of the FIFA to expand the competition. "My big concern is that as football itself changes, the attractiveness of the game suffers."
Smaller nations such as Scotland - who also backed the expansion of the European Championships to 24 teams - were more positive.
"We believe this is a positive step, particularly for the smaller nations, and will allow more fans across the globe to revel in their country’s participation at a FIFA World Cup Finals," Scottish federation chief executive Stewart Regan said.
"This will also allow these nations to invest further in their footballing infrastructure and youth development, which in turn can yield significant social benefits."
And though FIFA believes the current number of 12 stadiums will not need to be increased, the additional infrastructure required to host 48 teams means fewer countries can consider bidding for the event.
A North American bid, led by the United States, is considered the early favourite to host 2026 with Europe and Asia out of the running due to hosting the next events. A decision on the host is scheduled to be made in 2020.
The 2018 and 2022 World Cups in Russia and Qatar will remain with 32 teams.