Jokiharju arrived in North America in 2016 and played his first season with Portland of the Western Hockey League, scoring 48 points (nine goals, 39 assists) in 71 games.

That showing caught the attention of the Chicago Blackhawks, who selected the Oulu, Finland native with the No. 29 pick at the 2017 NHL Draft.

Following one more season in Portland, when he was named to the WHL West Second All-Star Team after he tied for third among league defensemen with 71 points (12 goals, 59 assists) in 63 games, Jokiharju made his NHL debut with the Blackhawks against the Ottawa Senators on Oct. 4, 2018.

Although Jokiharju enjoyed a fast start, including five assists in the next two games, he wound up splitting time between Chicago and Rockford of the American Hockey League. He finished the season with 12 assists in 38 NHL regular-season games.

On July 9, 2019, Jokiharju was traded to the Sabres for forward Alexander Nylander.

During his first season with Buffalo, Jokiharju received more of an opportunity and scored 15 points (four goals, 11 assists) in 69 games before the NHL paused the 2019-20 season March 12 due to concerns surrounding the coronavirus.

Jokiharju signed a one-year, $3.1 million contract to stay with the Sabres on July 5, 2024. He led the Sabres the previous season with a plus-14 rating and ranked fourth on the team with 106 blocked shots. He was named to Finland's roster for the 4 Nations Face-Off as an injury replacement for Toronto Maple Leafs defenseman Jani Hakanpaa and helped Team Finland win bronze at the Olympic Winter Games Milano Cortina 2026.

Jokiharju was traded to the Boston Bruins on March 7, 2025, for a fourth-round pick in the 2026 NHL Draft. He signed a three-year, $9 million contract with Boston on June 30.