In 2018, Holmberg was drafted 156th overall by the Maple Leafs in the NHL entry draft after the team traded for the opportunity to select him.
In 2018, Pontus Holmberg made his debut for the Växjö Lakers in the Swedish Hockey League (SHL), playing two games.
In 2019, Holmberg was selected for Sweden's junior team at the World Juniors, where they were upset by Switzerland in the quarterfinals.
In the 2020 season, the Växjö Lakers were the top team in the regular season.
On June 4, 2021, Holmberg was signed by the Maple Leafs to a two-year, entry-level contract and was loaned back to the SHL's Växjö Lakers, later playing six games for the Toronto Marlies, scoring two goals and four points.
In 2022, Holmberg joined the Maple Leafs for training camp, was later demoted to the Toronto Marlies, and then recalled to the Maple Leafs.
In 2023, Holmberg participated in the Maple Leafs' training camp but was assigned to the Marlies to begin the season and later recalled on October 20 after Tyler Bertuzzi was injured.
At the conclusion of the 2024-25 season, the Maple Leafs chose not to extend a qualifying offer to Holmberg.
In 2024, Holmberg made the Maple Leafs out of training camp, playing on the third line.
In 2024, Holmberg won a bronze medal at the IIHF World Championship, playing on a line with Lucas Raymond and André Burakovsky and registering six assists in ten games.
On July 1, 2025, Holmberg signed a two-year deal with the Tampa Bay Lightning, carrying an average annual value of $1.55 million.
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