Jokinen has represented his native Finland on numerous occasions. He first played with the Finnish national junior team at the under-18 level in the 1996 European Junior Championship. He joined the under-20 team one year later for the 1997 World Junior Championship, scoring five goals in six games. He made his debut with the senior team that same year, finishing second in team scoring with six points in eight games at the 1997 World Championship.

The NHL’s Central Scouting Bureau rated Jokinen as the top European prospect for the 1997 NHL Entry Draft. He was selected by the Los Angeles Kings with the third overall selection, after Joe Thornton and Patrick Marleau. Jokinen began the 1997–98 season with the Kings, making his NHL debut on October 1, 1997, against the Pittsburgh Penguins. He was held pointless in eight games, however, and the Kings chose to return him to HIFK to complete the season.

Jokinen played 30 games with HIFK, scoring 39 points. He added another nine points in nine playoff games as the team won the SM-liiga championship. He won the Matti Keinonen and Jari Kurri trophies in 1998 as the most effective player of the regular season and most valuable player of the playoffs, respectively. He also scored the game-winning goal in game 3 in overtime vs Ilves to secure the championship for his team.

Returning to North America, Jokinen began the 1998–99 season with the Kings’ American Hockey League (AHL) affiliate, the Springfield Falcons. He earned a recall to Los Angeles after nine games, in which he scored nine points. He recorded his first NHL point on November 5, 1998, with an assist in a game against the St. Louis Blues, then scored his first NHL goal five nights later against the Calgary Flames. Jokinen was named the NHL’s Rookie of the Month for November, scoring eight points in 11 games. He finished the season with 21 points in 66 games played. Following the conclusion of the season, on June 20, 1999, Jokinen was traded to the New York Islanders, along with Josh Green, Mathieu Biron and a first-round selection at that year’s draft, in exchange for Žigmund Pálffy, Bryan Smolinski, Marcel Cousineau and a fourth-round selection. Jokinen was considered the central piece of the deal from New York’s perspective, as they gave up their top player in Pálffy.

At the 1998 World Junior Championship, Jokinen tied with American Jeff Farkas as the tournament’s scoring leader with ten points and helped Finland win the gold medal on home soil. He was named a tournament all-star at centre, and was given the Directorate Award as top forward. He then won a silver medal at the 1998 World Championship. Another silver followed in 1999 and bronze medals in 2000, 2006 and 2008. In total, Jokinen has appeared in ten World Championships for Finland, scoring 41 points in 82 games.

Jokinen played only one season on Long Island. He appeared in all 82 games for the Islanders, scoring 21 points. However, he was included in a trade at the 2000 NHL Entry Draft, as he was packaged with goaltender Roberto Luongo and sent to the Florida Panthers in exchange for Mark Parrish and Oleg Kvasha on June 24, 2000.

Jokinen met his wife Katerina, who was born in Greece but grew up in Finland, when they were both 18. They were married in 2001, and have three daughters.

Jokinen was named an alternate captain of the Panthers prior to the 2002–03 season, and was elevated to captain to begin 2003–04. He again led the team in goals (26) and points (58) and scored his 200th career point on March 10, 2004, with an assist against the Buffalo Sabres. When the 2004–05 season was cancelled due to a labour dispute, Jokinen played for several European teams: first EHC Kloten of the Swiss National League A, then Södertälje SK of the Swedish Elitserien and finally HIFK back in Finland. Returning to the NHL in 2005–06, Jokinen reached new career highs with 38 goals, 51 assists and 89 points. He played his 500th NHL game on November 19, 2005, against the New York Islanders, and recorded his first NHL hat-trick on November 25 against Pittsburgh.

At the 2006 Olympics in Turin, Jokinen tied with Teemu Selänne for the team lead with six goals and helped Finland reach its first gold medal game in a Winter Games. He and his teammates had to settle for silver, however, following a 3–2 loss to rival Sweden in the final. Jokinen won a bronze medal at his third Olympics, the 2010 Vancouver Games. He scored two goals, including the game winner, in a 5–3 victory over Slovakia in the third place game.

The 2008–09 season began well for Jokinen, as he recorded 18 points in his first 21 games with the Coyotes. A shoulder injury suffered in November 2008, however, caused him to miss a game for the first time since 2002–03, ending his streak of consecutive games played at 397. He appeared in 57 games for the Coyotes but did not finish the season in Phoenix; the Calgary Flames acquired him, along with a third-round draft pick, on March 4, 2009, in exchange for Matthew Lombardi, Brandon Prust and Calgary’s first-round selection at the 2010 NHL Entry Draft.

Jokinen appeared in his 1,000th NHL game on January 1, 2012, a 5–3 loss to the Nashville Predators.

After becoming an unrestricted free agent on July 1, 2012, Jokinen signed a two-year, $9 million deal with the Winnipeg Jets a day later, on July 2. He was named an alternate captain of the team at the start of the lockout-shortened 2012–13 season. While he was a popular player with his Jets teammates, Jokinen was unable to provide the type of offensive performance the team expected. He recorded only seven goals and seven assists in 45 games. Following the season, Jokinen admitted that not playing in Europe during the lockout negatively impacted his fitness and play throughout the NHL season.

Jokinen returned to Winnipeg for the 2013–14 season and reached a pair of milestones early in the campaign. He recorded both his 400th assist and 700th point on October 13, 2013, in a 3–0 victory over the New Jersey Devils. He played in all 82 games for Winnipeg and recorded 18 goals and 43 points. However, he was also passed by Bryan Little and Mark Scheifele on the Jets’ depth-chart at centre. As a consequence, Winnipeg allowed Jokinen to leave via free agency. On July 20, 2014, he signed a one-year contract with the Nashville Predators worth $2.5 million.

On February 15, 2015, Jokinen, along with Brendan Leipsic and a first-round draft pick in 2015, were traded to the Toronto Maple Leafs in exchange for Cody Franson and Mike Santorelli. He wore number 11 in Toronto as opposed to his regular number 13, out of respect for the Maple Leafs’ great Mats Sundin, saying, “There’s only one No. 13 for the Maple Leafs and that’s the way it should be.”

After only six games played for Toronto, Jokinen was traded to the St. Louis Blues in exchange for forward Joakim Lindström and a conditional sixth-round pick in 2016 (Nicolas Mattinen). He played 8 games with the Blues before suffering a season-ending injury on March 6 against the Toronto Maple Leafs.

Jokinen quietly ended his playing career after the 2014–15 season and began working as a trainer at a Florida-based hockey academy he started with former teammates Tomáš Vokoun and Radek Dvořák in August, 2016. His retirement was made official on March 7, 2017, when he signed an honorary contract with the Florida Panthers to retire as a Panther.