A ninth-round selection (No. 264) by the Anaheim Ducks in the 2001 NHL Draft, Parenteau spent seven seasons in the American Hockey League, plus a short stint in the East Coast Hockey League, before landing a regular role in the NHL at the age of 27.

In junior hockey, Parenteau showed strong offensive instincts. In 2001-02 with Chicoutimi in the Quebec Major Junior Hockey League, the 6-foot, 198-pound forward scored 51 goals and 118 points in 68 games. The following season he was traded to Sherbrooke and finished with a combined 33 goals and 103 points in 59 games, adding eight goals and 19 points in 12 playoff games.

Parenteau's trek through the minor leagues began in 2003-04 with Cincinnati in the AHL, where he would spend two seasons. The Ducks traded Parenteau to the Chicago Blackhawks on Dec. 28, 2006, and though he was initially sent to Norfolk in the AHL, Parenteau made his NHL debut on Feb. 7, 2007 against the Vancouver Canucks, his first of five NHL games that season.

Parenteau would wait another two seasons before appearing in an NHL game again, this time with the New York Rangers after he was acquired on Oct. 11, 2007. While with Hartford, New York's AHL affiliate, Parenteau established himself as a top scorer, combining for 63 goals and 159 points from 2007-09, earning Second Team All-Star honors in 2008 and First Team All-Star honors in 2009.

But it wasn't until Oct. 28, 2009 that he would get another chance in the NHL when he made his Rangers debut, scoring his first career goal in a 3-1 loss to the New York Islanders. Parenteau finished the season with three goals and eight points in 22 games.

As a free agent, Parenteau signed with the Islanders and earned a full-time roster spot out of training camp, finishing the 2010-11 season with 20 goals and 53 points in 81 games. Following an 18-goal, 67-point season in 2011-12, he signed as a free agent with the Colorado Avalanche on July 1, 2012 and continued to produce. He scored a team-high 18 goals and tied for the team high with 43 points in the 48-game season in 2012-13.

Following two seasons with the Avalanche, Parenteau was traded to the Montreal Canadiens on June 30, 2014. Plagued by injuries that limited him to 56 games and just 22 points, the Canadiens exercised a buyout on the remaining year of Parenteau's contract on June 29, 2015.

Parenteau signed a one-year contract with the Toronto Maple Leafs as a free agent on July 1, 2015, and rebounded with a 20-goal season in 77 games. After one year with the Maple Leafs, Parenteau signed as a free agent for a second stint with the Islanders on July 2, 2016.