The tournament will feature clubs from each of the six confederations, with Europe entering 12 teams.
Chelsea, Real Madrid and Manchester City have qualified automatically as the most recent Champions League winners in the four-year cycle.
Bayern Munich, Paris St-Germain, Inter Milan, Porto and Benfica have also secured places in the tournament in 2025 via the coefficient pathway.
FIFA president Gianni Infantino confirmed the news at a meeting in Jeddah, Saudi Arabia on Sunday.
The revamped format will be played in the same slot where FIFA has previously held the Confederations Cup for international teams, a year before the World Cup.
Football’s world governing body said the summer dates had been set to ensure the scheduling aligns with the international match calendar, and to allow sufficient rest time before the start of the domestic seasons.
The powerful European Clubs’ Association has backed the tournament but Maheta Molango, head of the Professional Footballers’ Association, said FIFA’s persistence to go ahead with the expansion shows a lack of concern for player welfare.
“Players have become pawns in a battle for primacy between football’s governing bodies,” he added. “With no-one willing to take a step back or to work collaboratively to create a sustainable calendar.
“These decisions have consequences – not just for players who are being pushed until they break. But for the future quality of these tournaments, with players becoming injured or withdrawing from games as they make their own decisions about how to manage what have become ridiculous demands.”
In a statement, Fifpro, the world players’ union, said there was also “a disregard” for players’ “personal and family lives”.
It added: “The expanded competition will undercut the rest and recovery time of these players at the end of the 2024-25 season, and further disrupt national employment markets by changing the balance between national and international competitions.
“Players will have to perform at the end of an 11-month season with little prospect of getting enough rest before the following season starts.
“The extreme mental and physical pressures at the pinnacle of the game is the principal concern of players with multiple club and national team competitions, leading to exhaustion, physical injuries, mental health issues, diminished performance, and risks to career longevity.”
FIFA also announced a new Intercontinental Cup competition from December 2024, which will see the winners of the Champions League face a team that comes through intercontinental play-offs.