May 23, 2017 0657 GMT
In a bid to widen the game's global appeal and enrich its coffers, the FIFA panel endorsed a format with 16 groups of three nations, a tweet from FIFA's official account said, AFP reported.
The move represents the first major change to the World Cup since the tournament was boosted from 24 to 32 teams for the 1998 tournament in France.
Critics strongly oppose the move and it was branded a "money grab and power grab" by New FIFA Now, a group campaigning for reform of the scandal-tainted FIFA.
Infantino took over the body 11 months ago with a vow to repair the damage done at the end of Sepp Blatter's tenure by growing football across the globe.
Enlarging the World Cup, the planet's top sporting competition, was the centerpiece of that plan.
Critics say the expanded tournament would dilute the quality of play and overburden already exhausted players.
Football's powerful European Club Association reiterated its opposition, describing the 32-team model as "the perfect formula".
"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," the body which represents European football clubs said in a statement.
Despite the opposition Infantino had in recent weeks voiced confidence that his flagship project would be approved, noting it would improve FIFA's bank account.
And a confidential FIFA report seen by AFP projects a 48-team tournament would bring a cash boost of $640 million (€605 million) above projected revenues for next year's finals in Russia.
But Infantino has also argued that more World Cup berths would help serve football's interest by boosting "inclusion" in the "biggest social and sporting event".
Among those who seemed convinced by that argument was Argentine football legend Diego Maradona, who on Monday said a 48-team format "will give more possibilities to countries that have never reached that level of competition".
Africa and Asia could be the big winners with a rise in their number of places — currently at five for Africa and between four and five for Asia.
But in order to smooth over skepticism about World Cup reform within UEFA, it is likely that Europe will also see its allotments rise above the current 13 places.
A source close to FIFA told AFP that under the new format Europe could get 16 places, with Africa earning nine.
But that information remained unconfirmed and world football's governing body was not expected to immediately announce its final decision on allotments, which may fuel a tough debate in the months ahead.
The council officially weighed five proposals during Tuesday's meeting at FIFA's snow-covered Zurich headquarters, including maintaining the status quo of 32-teams.
The landmark decision to expand the tournament is the latest overhaul of the World Cup, which has seen its global popularity and financial might surge since the inaugural edition in 1930.
That contest, won by Uruguay, had just 13 countries.
The World Cup expanded to 24 teams in 1982 in Spain before moving to its current 32-team version at France 1998.
80 matches, 32 days
Earlier World Cup enlargement plans foresaw a longer tournament, which raised alarm that international football's already stretched calendar would be further tested.
The format approved Tuesday envisages 80 matches — 16 more than the current set up — but crucially will still be played over the same 32 days.
Two teams from each group will advance to a 32-nation knockout round.
Some have pointed to Euro 2016 — which expanded to 24 nations — as evidence that competition can remain fierce with more countries involved, noting the stunning achievements of football minnows like Iceland and Wales.
Bidding to host the 2026 tournament has not yet opened, but Infantino has voiced support for two countries sharing the duty, easing the financial burden on a single host nation.
Sources close to FIFA have said that a joint US-Canada bid, possibly involving Mexico could emerge, while Morocco has also been mentioned.