The World Cup will be expanded to host 48 teams, up from 32, Fifa has decided.
An initial stage of 16 groups of three teams will precede a knockout stage for the remaining 32 when the change is made for the 2026 tournament.
The sport's world governing body voted unanimously in favour of the change at a meeting in Zurich on Tuesday.
The number of tournament matches will rise to 80, from 64, but the eventual winners will still play only seven games.
The tournament will be completed within 32 days - a measure to appease powerful European clubs, who objected to reform because of a crowded international schedule.
The changes mark the first World Cup expansion since 1998.
Why expand? 'Football is more than just Europe and South America'
Fifa president Gianni Infantino has been behind the move, saying the World Cup has to be "more inclusive".
"We are in the 21st century and we have to shape the World Cup of the 21st century," he said at a news conference after the announcement.
"It is the future. Football is more than just Europe and South America, football is global.
"The football fever you have in a country that qualifies for the World Cup is the biggest promotional tool for football you can have.
"This football promotion, in many parts of the world where today they have no chance to play [at the World Cup], was at the top of our thoughts."
According to Fifa research, revenue is predicted to increase to £5.29bn for a 48-team tournament, giving a potential profit rise of £521m.
Campaign group New Fifa Now described the expansion as "a money grab and power grab".
But Infantino said: "It's not at all a money and power grab, it is the opposite, it's a football decision."
He added the decision was taken "based on sporting merit".
He says the decision on who will get the extra qualification slots has yet to be decided but "this will be looked at speedily".
"No guarantees have been made," he added. "The only sure thing is that everyone will have a bit more [representation] than they have."
He says there is no rush to decide what will be used to separate teams who finish on the same points and goal difference. Reports had suggested there could be a penalty shootout at the end of each drawn match.
But Infantino said: "This will be part of the regulations to be decided a few years before the event, it is nothing for now."
FA wants further information
The Football Association said in a statement: "We will work with Uefa, Fifa and the other European associations to understand how the 48-team Fifa World Cup will work.
"The priority has to be consideration of the potential impact on fans, players, teams and leagues, and also recognition of the importance of sporting integrity and commercial viability.
"In terms of the allocation of places, we note that further discussions will follow across the confederations and would expect a proper consultation process to be carried out before any decision is made."
Scottish Football Association chief executive Stewart Regan welcomed the expansion, saying it was a a "positive step, particularly for the smaller nations".
Uefa, European football's governing body,said: "It was clear that all other confederations were overwhelmingly in favour of expanding the Fifa World Cup to 48 teams. As a result, Uefa decided to join in supporting the new format of the competition.
"Uefa is satisfied that it succeeded in postponing the final decision regarding the slot allocation of every confederation in the future format of the Fifa World Cup.
"We would also like to state that we are happy that the new proposed length and format of the tournament does not increase the burden on players. We will also ensure that clubs' interests will continue to be protected."
What the critics say: 'It will dilute the competitiveness'
The European Club Association (ECA), which represents the interests of clubs at European level, reiterated it was not in favour of an expansion. It said Fifa had made a political rather than sporting decision.
"We fail to see the merits to changing the format of 32 that has proven to be the perfect formula from all perspectives," it said in a statement.
"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.
"ECA will analyse in detail the impact and the consequences of the new format and will address the matter at the next meeting of its executive board, scheduled for the end of January."
New Fifa Now says the governing body needs to reform, said it would "dilute the competitiveness of the tournament".
"It will not help development of the game or provide improved competitive opportunities for lower-ranked nations," it added. "Instead, it will make a mockery of the qualification process for most confederations."
History of World Cup overhauls
|1930 Uruguay||13||1 group of 4 and 3 groups of 3, with only top team progressing to semi-finals|
|1934 Italy||16||Straight knockout tournament|
|1950 Brazil||15 (13 took part)||3 groups of 4 and 1 group of 3, with top side progressing to final group of four|
|1954 Switzerland||16||4 groups of 4, but only 2 games in each group, with top 2 sides through to quarter-finals|
|1958 Sweden||16||4 groups of 4, this time with 3 games. Top 2 sides through to quarter-finals|
|1974 West Germany||16||4 groups of 4 but now followed with 2 groups of 4, the 2 top sides competing the final|
|1982 Spain||24||6 groups of 4 followed by 4 groups of 3, the winner of each qualifying for the semi-finals|
|1986 Mexico||24||6 groups of 4, top 2 sides and 4 best 3rd-placed teams qualifying for round of 16|
|1998 France||32||8 groups of 4, top 2 sides progressing to knockout rounds|