Selected by the Carolina Hurricanes in the third round (No. 67) of the 2014 NHL Draft, Foegele had a goal and an assist in his debut against the Ottawa Senators on March 26, 2018.

After playing most of his first professional season (2017-18) with Charlotte of the American Hockey League, Foegele became a full-time NHL player in 2018-19 and scored 15 points (10 goals, five assists) in 77 games. He then had nine points (five goals, four assists) in 15 Stanley Cup Playoff games to help the Hurricanes reach the Eastern Conference Final.

Foegele became the fifth player in Hurricanes/Hartford Whalers history to score two shorthanded goals in one game during a 4-0 win against the Calgary Flames on Dec. 14, 2019.

On July 28, 2021, the Hurricanes traded Foegele to the Edmonton Oilers for defenseman Ethan Bear. He had a five-point game (two goals, three assists) in Edmonton's 7-2 win at the Anaheim Ducks on Dec. 31, 2023, and became the first Oilers player with five even-strength points in a game since Sam Gagner in an 8-4 win against the Chicago Blackhawks on Feb 2, 2012.

Foegele signed a three-year, $10.5 million contract with the Los Angeles Kings on July 1, 2024. He had 20 goals and 41 points in 82 regular-season games for the Oilers the prior season and eight points (three goals, five assists) in 22 playoff games to help them advance to the Stanley Cup Final, a seven-game loss to the Florida Panthers.

He scored 24 goals in 82 games of his first season in Los Angeles, had his 100th NHL assist in a 6-5 win at the Vegas Golden Knights on March 9, 2025, and was honored with the Kings' Mark Bavis Memorial Award for Best Newcomer and the Unsung Hero Award.

Foegele was traded to the Ottawa Senators on March 5, 2026.