In the National Hockey League (NHL) he played for the Chicago Blackhawks, New York Rangers, New York Islanders, Colorado Avalanche, Montreal Canadiens, Toronto Maple Leafs, New Jersey Devils and Nashville Predators, and then finished his career with Avtomobilist Yekaterinburg of the Kontinental Hockey League (KHL).

On December 28, 2006, Parenteau was traded from the Ducks, along with Bruno St. Jacques, to the Chicago Blackhawks in exchange for Sébastien Caron, Matt Keith and Chris Durno.

[3] With two more extended stints with the Rangers throughout the season, Parenteau posted eight points in 22 games, producing enough league-wide interest to earn him a free agent contract from the New York Islanders for one-year on July 2, 2010.

Parenteau made the Islanders' opening night roster out of training camp and found a permanent spot on the top line alongside John Tavares and Matt Moulson.

[6] With the lock-out-shortened 2012–13 season delaying his Colorado debut, Parenteau later scored his first goal for the Avalanche in a 3–1 home opening victory over the Los Angeles Kings on January 22, 2013.

[9] In participating in every game for the Avalanche that season, he recorded a career-best points-per-game average to lead the team with 18 goals and co-lead, alongside linemate Matt Duchene, with 43 points.

[17] On July 3, 2016, Parenteau signed a one-year deal with the New York Islanders, a team he had previously played for between 2010 and 2012,[18] but was waived on October 10, 2016.

Parenteau as a free agent from the Predators, was unsigned over the summer before agreeing to a professional tryout contract with the Detroit Red Wings on September 6, 2017.

On November 1, 2017, he signed for the remainder of the 2017–18 season with Russian outfit, Avtomobilist Yekaterinburg of the Kontinental Hockey League (KHL).