The FIFA Council have unanimously approved a 48-team World Cup from 2026 at a vote in Zurich.
The plans overseen by president Gianni Infantino mean the tournament will now have 16 groups of three teams.
Infantino has also suggested FIFA could also introduce penalty shoot-outs after group matches that end in a draw in order to stop teams playing for a result that favours them both.
The top two sides in each of the 16 groups will advance into a last-32 knock-out stage. There will be a total of 80 games in the tournament. Currently, in the 32-team format, 64 matches are played overall.
There were also options for the 37-member council to vote for a 40-team tournament, with 10 groups of four or eight groups of five, but the only other 48-team proposal saw a 32-team one-game knockout round with the winners joining 16 already-qualified teams.
European places at the competition will rise from 13 to 16. Africa are set for nine spots rather than five and Asia will also benefit, receiving four extra entries for the competition.
The other major decision regarding 2026 – who will host the event – 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, an early favourite.
Infantino’s expansion plans have been fiercely criticised but have also gained backing from the likes of Jose Mourinho and Diego Maradona.
Maradona said: ‘I’m delighted by Gianni’s initiative because it gives chances to teams that otherwise would start the qualifiers knowing they had no chance of getting to the World Cup.
‘It gives each country the dream and it renews the passion for football, it appears to me to be a fantastic idea.’