Growing up in Winkler, Manitoba, Penner played for his high school hockey team, the Garden Valley Collegiate Zodiacs, alongside future Washington Capitals teammate Eric Fehr. After high school, he was cut by many minor hockey teams, including his local junior club three times.
With little hope of ever playing hockey professionally, Penner agreed to play with Minot State University-Bottineau, now known as Dakota College at Bottineau, but immediately broke his femur, ending his first year with the club. The next year, in the 2001–02 season, he became a very important player for Bottineau, scoring 20 goals with 13 assists in 23 games, also earning the Most Determined Player Award for his improvement and stellar play after recovering from his injury.
Penner then went to an evaluation camp at Saskatoon. He played well there, scoring an average of three points per game. He was scouted by Grant Standbrook, the assistant coach for the University of Maine, and was offered a scholarship, which he accepted. Although he did not initially join the team, in the 2003–04 season, he helped lead the Black Bears and to the NCAA Championship game, scoring the game-winning goal in the semi-finals against Boston College. Maine then lost the championship title game to the University of Denver 1–0.
Penner was signed as a free agent by the Mighty Ducks of Anaheim on May 12, 2004, to a three-year entry-level contract. He was assigned to the Cincinnati Mighty Ducks, Anaheim's American Hockey League (AHL) affiliate. He recorded 28 points in his professional rookie season with Cincinnati, then took a major step the next season as he was moved to the Portland Pirates, who became the Mighty Ducks' AHL affiliate in 2005–06. He scored 39 goals and 84 points in 57 games with Portland while also making his NHL debut, appearing in 19 games with the Mighty Ducks that season. He was originally called up on November 23, 2005, being sent back and forth from the minors. During the Mighty Ducks' 2006 playoff run, Penner scored nine points in 13 games until Anaheim was eliminated by the Edmonton Oilers in the Western Conference Finals.
Penner earned a full-time roster spot with the Ducks in 2006–07 and broke out with 29 goals and 45 points playing with Ryan Getzlaf and Corey Perry on a unit dubbed the "Kid Line." Penner's goal total was the second-highest on the team, only trailing superstar Teemu Selänne. He also set the Ducks' franchise rookie record for most points (surpassed by Bobby Ryan in 2008–09). During the Ducks' 2007 Stanley Cup run, Penner scored the game-winner in Game 1 of the Western Conference Quarter-finals against the Minnesota Wild and Game 4 of the Stanley Cup Finals against the Ottawa Senators. In Game 5, Penner and the Ducks defeated the Senators 6–2 to win the Stanley Cup. Penner became the first former Maine Black Bear to win the Stanley Cup as a player.
After winning the Stanley Cup with the Ducks, Penner's entry-level deal expired and he became a restricted free agent in the off-season. With the Ducks dealing with salary cap issues and the signing of Todd Bertuzzi, Edmonton Oilers General Manager Kevin Lowe jumped at the opportunity and signed Penner to a five-year, $21.25 million offer sheet. Lowe was criticized by the media and specifically Ducks' General Manager Brian Burke. After seven days had passed, the Ducks were ultimately unwilling to match the offer and Penner became an Oiler. To date, Penner is the most recent player to change teams via an offer sheet.
In his first season with the Oilers, Penner scored a team-high 23 goals and improved to 47 points. He then began the 2008–09 season with a slow start and was publicly criticized by Head Coach Craig MacTavish for a lack of fitness and competitiveness after being made a healthy scratch for the second consecutive game.
Penner was confirmed to be a part of a planned summertime 2009 blockbuster trade that would see Andrew Cogliano, Ladislav Šmíd and himself dealt to the Ottawa Senators in exchange for disgruntled All-Star forward Dany Heatley. In the end, however, Heatley exercised the no-trade clause contained in his contract and the deal could not be finalized (Heatley would, shortly after, accept a trade to the San Jose Sharks).
Penner got off to a good start in 2009–10 season and was fourth in NHL scoring with 11 goals and 11 assists after 18 games played. On October 22, for the first time in his career, he scored five points (two goals and three assists), in a game against the Columbus Blue Jackets. His linemates for that game were Aleš Hemský (one goal and four assists) and Sam Gagner (one goal and two assists). At season's end, the Oilers had finished last overall in the league, but Penner had recorded career highs in goals (32) and points (63).
On February 28, 2011, Penner was traded from Edmonton to the Los Angeles Kings in exchange for Colten Teubert, a first-round draft pick in 2011 (Oscar Klefbom), as well as a conditional third-round pick in the 2012 (Daniil Zharkov).
On January 7, 2012, Penner experienced back spasms while attempting to eat some self-described "delicious pancakes", an injury that caused him to miss a game and become the subject of pancake-related jokes among fans.
On May 22, 2012, Penner scored the winning goal in overtime in Game 5 against the Phoenix Coyotes to advance the Kings to the 2012 Stanley Cup Finals. On June 11, 2012, Penner won his second Stanley Cup, as the Kings defeated the New Jersey Devils 6–1 in Game 6.
Penner is only the 21st NHL player to play for both sides of the Freeway Face-Off between the Anaheim Ducks and the Los Angeles Kings—and the only one to win the Stanley Cup with both teams.
Penner re-signed with the Kings on July 1, 2012, to a one-year contract worth $3.25 million.
On July 16, 2013, Penner was signed as a free agent to return on a one-year, $2 million deal with the Anaheim Ducks. During the 2013–14 season, Penner rebounded offensively with the Ducks, reuniting with former line-mates Ryan Getzlaf and Corey Perry.
In 49 games with Anaheim, Penner scored 13 goals and 32 points before he was dealt approaching the trade deadline to the Washington Capitals in exchange for a fourth-round pick on March 4, 2014.2001-02 - NJCAA - Most Determined Player Award - MSU-Bottineau
2003-04 - NCAA - Jack Semler Award, University of Maine (Most Improved Player)
2006-07 - NHL - Stanley Cup (Anaheim Ducks)
2011-12 - NHL- Stanley Cup (Los Angeles Kings)
May 12, 2004 - Dustin Penner was signed as a free agent by the Mighty Ducks of Anaheim.
August 2, 2007 - Signed as a restricted free agent by the Edmonton Oilers to an offer sheet that was not matched by the Anaheim Ducks. The Ducks received 1st, 2nd, and 3rd round picks from the Edmonton Oilers as compensation in the 2008 NHL Entry Draft.
February 28, 2011 - Traded to Los Angeles Kings.
July 1, 2012 - Resigned with the Los Angeles Kings as an unrestricted free agent.
July 16, 2013 - Dustin Penner returned to the Anaheim Ducks as an unrestricted free agent.
March 4, 2014 - Traded to the Washington Capitals.