President Gianni Infantino's proposal was rubber-stamped on Tuesday, with the 2026 tournament set to feature 16 groups of three teams.
It is the first time since 1998 that changes have been made to the make-up of a competition that originally comprised just 13 teams, but how will they work in practice and who could now get an invite to world football's showpiece event? Here's what you need to know.
How will the new format work?
Delegates voted on four different options to expand the World Cup - including 40 teams in groups of four or five - but emphatically backed Infantino's preference for 48 sides in 16 groups of three, followed by a 32-team knock-out.
The winning format will increase the number of games from 64 to 80 but see the tournament completed inside the current 32-day schedule.
Why did FIFA want change?
Infantino repeatedly said his main motivation for expansion was to give more nations a chance of experiencing the joy of a World Cup, bolstering international football in developed markets and helping its growth in new ones.
"FIFA's idea is to develop football in the whole world," Infantino said when he suggested the idea in October. "The World Cup is the biggest event there is. It's more than a competition, it's a social event."
Critics argue that the expansion proposal was driven by money; FIFA predict that revenues could rise to £5.3billion compared to £4.5bn for the 2018 World Cup in Russia.
The proposal was also an early test of Infantino's fledgling administration. The man who went on to replace Sepp Blatter made World Cup reform a key election pledge back in February and it was always likely to appeal; 135 of FIFA's 211 member associations have never played at a World Cup.
Who stands to benefit?
It's yet to be decided how the 16 extra places at the World Cup in 2026 will be allocated but one proposal under review is for Europe to have an additional three teams.
Africa would have an extra four and six South American teams would automatically qualify. Oceania would have a guaranteed finalist, while there would be a play-off between one of the Asian teams and one from the CONCACAF Federation.
Euro 2016 heroes Iceland plus the likes of Uzbekistan, Burkina Faso and Venezuela - all sides who have come agonisingly close to the finals - could finally book their place in 2026 but the picture could become clearer after the FIFA Council's next meeting in Bahrain in May. One thing is certain: there'll be a scramble for places.
Who's for and who's against?
The pressure group New FIFA Now, which has campaigned for reform of FIFA, has already criticised the news, declaring the changes a "money grab".
"It will not help development of the game or provide improved competitive opportunities for lower-ranked nations," it said in a statement. "Instead, it will make a mockery of the qualification process for most confederations ... it is a money grab and power grab.
The influential European Club Association - of which Manchester United and Liverpool are members - also issued a strong statement, suggesting the decision was based on "political reasons rather than sporting ones".
Germany have been vociferous critics of World Cup reform but the majority of European football nations have supported the plans.
Scottish FA chief executive Stewart Regan welcomed the news, saying: "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. This will also allow these nations to invest further in their footballing infrastructure and youth development, which in turn can yield significant social benefits."
England's Football Association backed Infantino's presidency bid but, speaking recently, Martin Glenn, the FA's chief executive officer, admitted to reservations about the FIFA chief's blueprint.
"I can't influence FIFA," Glenn said earlier this month. "Our preference would be to keep the tournament smaller, because there's a quality factor here, but we'll try to influence the shape of it."
What's still to be decided?
As part of his overhaul plans, Infantino has further suggested that penalty shoot-outs be brought in to settle the results of all drawn games, thereby minimising the risk of teams colluding in their final games to eliminate others from the tournament.
The other major decision regarding 2026 is who will host the event. That is not scheduled for consideration until 2020 with a bid featuring the United States, either on its own or in conjunction with one or both of Canada and Mexico, the overwhelming favourite.