Professional
After leading the Spartans in both points and as captain in the 2005–06 season, Miller signed a two-year entry-level contract with the Ducks on May 4, 2006. He joined Anaheim's AHL affiliate, the Portland Pirates, during their second round series against the Hartford Wolf Pack, playing in one game.
The next season, he suited up for 79 matches with the Pirates, scoring 16 goals and totaling 20 assists for 36 points to place third on the team.
In 2007, Miller once again moved up to a higher league after completing the regular season with another team. On April 16, Miller was recalled from Portland by Anaheim. Three days later, he made his Ducks and NHL debut at the Honda Center, playing in what would be the final game of the Western Conference Quarterfinal series against the Minnesota Wild.
Coach Randy Carlyle placed the left winger on the Ducks' top line, alongside 2007 All-Stars Andy McDonald and Teemu Selänne, to fill in for the injured Chris Kunitz. In game one, Miller forced a turnover that Selanne and McDonald capitalized on for the Ducks' first goal of the series. He would also play in the Stanley Cup Final and would go on to win his first Stanley Cup after just three games in the NHL.
He would spend two more seasons in the Ducks organization before being traded to the Tampa Bay Lightning in the summer of 2009 for Russian winger Evgeny Artyukhin. Miller went scoreless in 14 games with the Lightning that season.
On November 10, 2009, Miller was put on waivers by the Lightning and was subsequently claimed by the Detroit Red Wings. He made his Red Wings debut on November 12 against the Vancouver Canucks, recording 11:33 minutes of ice time. He scored his first goal in a Detroit uniform on November 23 against the Nashville Predators. Originally brought into Detroit to replace injured players on a temporary basis, he effectively outplayed other young members of the Red Wings. He has since filled in comfortably playing a variety of roles. He finished the 2009–10 season with 10 goals, and 9 assists (zero points with the Lightning) in 80 games split between the Lightning and Red Wings.
During the summer of 2010 the Red Wings re-signed Miller to a one-year $650,000 contract. During the 2010–11 season Miller played 68 games, scoring 10 goals, and eight assists. He played the role of a grinder, spending time primarily on the third and fourth lines, while also contributing on the penalty kill. Most games Miller would play on a line with Justin Abdelkader, Darren Helm, Patrick Eaves and/or veteran Kris Draper. This would alter game to game depending on injuries, and or the matchups coach Mike Babcock saw fit in that particular game.
Following his season, the Red Wings rewarded Miller's efforts by re-signing him to a two-year contract worth $1.675 million on July 1. Each year has an annual cap hit of $837,500. On February 19, 2012, Miller scored his career high 12th goal of the regular season against the San Jose Sharks in a 3–2 Red Wings victory.
During the 2012 NHL lockout, Miller signed with the British Elite Ice Hockey League club Braehead Clan.
On June 29, 2013, Miller signed a three-year, $4.05 million contract extension with the Detroit Red Wings.
On March 31, 2015, Miller suffered two lacerations, one on his right cheek, and one above his right eye, after the skate of Mark Stone of the Ottawa Senators struck him in the face. The four-inch long cut required 60 stitches to close the lacerations. He did not sustain damage to his eye or his vision.
Miller finished the 2014–15 season with five goals and eights assists in 82 games. He led all NHL forwards and established a career high in blocked shots during the regular season with 99. This is the highest single-season total in blocked shots by a forward in the past seven seasons. He has led all Red Wings forwards in blocked shots for five straight seasons.
On December 3, 2015, Miller suffered a broken jaw in a game against the Arizona Coyotes. He returned on January 7, 2016, after missing 14 games, however, the comeback lasted less than two games as Miller was hurt in the third period against the Anaheim Ducks on January 10, by a hit by Shea Theodore. It was announced that Miller had to have left ACL reconstruction in addition to meniscus repair and would be out for 4 to 6 months. During the 2015–16 season, Miller recorded one goal and one assist in 28 games. On June 27, 2016, the Red Wings signed Miller to a one-year contract extension. The Red Wings chose not to re-sign Miller following the conclusion of his contract, making him an unrestricted free agent after 8 years with the organization.
On September 11, 2017, as a free agent over the summer, the Chicago Blackhawks signed Miller to a professional tryout. On September 21, 2017, Miller was released from the Blackhawks roster following training camp. Midway into the 2017–18 season, Miller signed for the remainder of the campaign with Swedish outfit, Brynäs IF of the SHL, on November 20, 2017.
