Pageau was selected by his hometown Ottawa Senators in the fourth round (No. 96) of the 2011 NHL Draft after he had 79 points (32 goals, 47 assists) in 67 games for Gatineau of the Quebec Major Junior Hockey League.

He played 69 games for Binghamton of the American Hockey League in 2012-13 but finished the season with Ottawa and had a hat trick against the Montreal Canadiens in Game 3 of the Eastern Conference Quarterfinals.

After playing 27 games for Binghamton in 2014-15, Pageau was recalled and played 50 games with Ottawa and had 19 points (10 goals, nine assists). He played all 82 NHL games the following season and had 19 goals and 43 points.

Pageau helped the Senators reach the 2017 Eastern Conference Final with eight goals and two assists in 19 Stanley Cup Playoff games. Approaching unrestricted free agency, he had 24 goals for the Senators when he was traded to the New York Islanders on Feb. 24, 2020. He immediately signed a six-year contract with New York and scored in his Islanders debut against the New York Rangers the following night.

Pageau's five short-handed assists in 2023-24 were second in the NHL and he became the first Islanders skater since Bryan Trottier in 1983-84 to achieve the feat. He had 28 assists in 2024-25, including his 200th in the NHL in a 4-2 win at the San Jose Sharks on March 28. He signed a three-year contract with the Islanders on March 6, 2026.