He spent his entire National Hockey League (NHL) career with the Detroit Red Wings, by whom he was drafted in 2003.

While at UMaine, Howard led the Black Bears to the 2003–04 Frozen Four championship game, losing 1–0 to the University of Denver.

[5] Beginning with the 2005–06 season, Howard began his career in the AHL with the Grand Rapids Griffins where he was occasionally called up to play for the Detroit Red Wings of the National Hockey League.

[2] He was in net for the Red Wings four times in the 2005–06 season posting a 1–2–0 record, a GAA of 2.99 and a save percentage of .904.

He recorded his first win of the 2009–10 season on October 27 in relief of Chris Osgood against the Vancouver Canucks, making 20 saves.

Howard won the 2010 Detroit Red Wings-Detroit Sports Broadcasters Association Rookie of the Year Award.

On February 28, 2011, Howard signed a two-year contract extension with the Red Wings worth $2.25 million per season.

[10] On January 23, 2012, in the Red Wings' 49th game, Howard recorded his 30th win of the season, before the All-Star break.

[16] On April 6, 2016, Howard recorded his 22nd shutout victory as a Red Wing against the Philadelphia Flyers in a 3–0 game at Joe Louis Arena moving him to fourth in franchise history.

[17] On February 14, 2019, Howard appeared in his 500th career NHL game, becoming the third Red Wings goalie to reach the milestone, following Terry Sawchuk and Chris Osgood.

[21] In September 2022 it was announced that Howard was hired as Red Wings studio analyst for Bally Sports Detroit during the 2022–23 season.

[2] He made his Senior international debut representing the United States at the 2012 World Championships, collecting five wins in seven games despite finishing in 7th place.