A Hobey Baker Award nominee and National Collegiate Athletic Association All-American while tending goal for University of Massachusetts Lowell, Roloson went undrafted after graduating. He was signed as a free agent by the Calgary Flames in 1994. After splitting time between the Flames and their American Hockey League counterpart, the Saint John Flames, he was traded to the Buffalo Sabres to back up Dominik Hasek. Following two years with the Sabres, he was picked up in the 2000 NHL Expansion Draft by the Columbus Blue Jackets. Rather than joining the Blue Jackets, Roloson signed with the AHL team of the St. Louis Blues, the Worcester IceCats.
Roloson earned a roster spot with the Minnesota Wild in 2001. In the 2002–03 NHL season, Roloson shared netminding duties with Manny Fernandez as the Wild made their first ever appearance in the post-season, reaching the conference final. Despite splitting goaltending duties with Fernandez, Roloson earned his first All-Star appearance at age 34, appearing in the 2004 NHL All-Star Game with the Western Conference team. He also won the Roger Crozier Saving Grace Award for having the NHL's best save percentage. During the 2004–05 NHL lockout, Roloson played with Finnish club, Lukko Rauma of the SM-liiga.
On March 8, 2006, Roloson was traded to the Edmonton Oilers in exchange for the first round pick that later became part of a trade for Pavol Demitra and a conditional draft pick that later became a third-rounder. Initially, Oilers General Manager Kevin Lowe was harshly criticized for the acquisition when Roloson struggled during the regular season. Lowe was criticized both for not acquiring a better goaltender, and also for surrendering a first-round draft pick to a divisional rival.
Criticism was muted following sensational play by Roloson, backstopping the Oilers to the final of the 2006 Stanley Cup Playoffs. He had a record of 12–5 through the first three rounds, and along with Chris Pronger, was considered a front-runner for the Conn Smythe Trophy if the Oilers were victorious in the finals.
However, during Game 1 of the Stanley Cup Finals against the Carolina Hurricanes, Roloson suffered a third-degree MCL sprain of his right knee when Hurricanes forward Andrew Ladd was pushed into Roloson by a back-checking Oiler defenseman Marc-Andre Bergeron. Oilers coach Craig MacTavish announced that Roloson would not be able to continue in the series. It was also learned that he had hyper-extended his right elbow in the collision as well. Backup Ty Conklin replaced Roloson for the remainder of Game 1 and co-backup goalie Jussi Markkanen finished the series. The Oilers lost to the Hurricanes in seven games. Months of intense rehabilitation would follow in order to prepare Roloson for the 2006–07 season.
Roloson could have tested the unrestricted free agency market in the summer of 2006 but opted to re-sign with the Oilers on July 1, 2006 for a three-year term.
In the 2007–08 season, Roloson started out strong before seeing his record fall to 7–12–0. By early January 2008, backup goaltender Mathieu Garon had taken the reins as starter. It wasn't until March 13, 2008, that Roloson saw regular play, coming in as relief for an injured Garon, starting each subsequent game.
When the 2008–09 NHL season began, Roloson found himself vying for the starting goaltender position with Garon and upstart Jeff Deslauriers. For the beginning of the season, it appeared Garon was once again the starter but after some bad games Oiler coach Craig MacTavish decided to rotate Garon, Deslauriers and Roloson by playing whoever had the hot hand. Eventually, the team traded Garon to the Pittsburgh Penguins and Roloson claimed the starting spot. Down the stretch, he started 36 consecutive games as the Oilers fought for a playoff spot. During this time, he became the oldest goaltender to start more than 60 games in a single season. Though the Oilers ultimately did not qualify for the post-season, Roloson put up solid numbers, making upwards of 40 saves on a regular basis.
On July 1, 2009, Roloson became an unrestricted free agent. After rejecting a one-year, $3-million deal from Edmonton, Roloson signed a two-year, $5-million contract with the New York Islanders. The Islanders also signed Martin Biron, who was to serve as Roloson's backup goalie while Rick DiPietro was out on injured reserve. Roloson lost his first game as an Islander on October 3, 2009 in a shootout.
On November 23, 2009, Roloson made 58 saves on 61 shots in a 4–3 overtime win in Toronto. The 58 saves were a career high, and broke the Islander club record of 56, held by Rick DiPietro.
On January 1, 2011, Roloson was traded to the Tampa Bay Lightning in exchange for defenceman Ty Wishart. He won his first game with Tampa Bay in a 1-0 overtime shutout against the Washington Capitals. In his first 11 games with the Lightning, he recorded 4 shutouts. In April 2011, Roloson recorded a shutout in a first round playoff Game 7 against the Pittsburgh Penguins, making him the oldest goaltender to do so. Roloson and the Lightning ultimately advanced to the 2011 Eastern Conference Finals, where they were eliminated by the Boston Bruins in seven games. With his contract set to expire the Lightning re-signed Roloson to a one-year $3 million deal on June 29, 2011. He retired at season's end after the Lightning failed to qualify for the playoffs again.
Roloson was a member of the Canadian 2007 IIHF World Championship team that won gold in a 4–2 win against Finland in Moscow.
In 2009, Roloson (along with Oilers teammate Shawn Horcoff) was called upon for Team Canada at the IIHF World Championships. He played in the finals against Russia, where Canada lost 2–1.
Following his retirement from ice hockey, Roloson was immediately hired as a consultant to the Anaheim Ducks farm team the Norfolk Admirals. On June 10, 2013, Roloson was named as the replacement for Pete Peeters as the Anaheim Ducks goaltending consultant. On November 2, 2014, he suited up in an emergency role after Ducks goaltender John Gibson suffered an injury pregame and could not play the game against Colorado.
Roloson and his wife, Melissa, who were married in 1999, have two sons, Brett and Ross. He is close friends with Rob Blake, with whom he played hockey in high school in Simcoe, Ontario. He is also friends with Andrew Brunette
The Saint Paul Police Federation swore in Dwayne Roloson as an honorary police officer for his interest and involvement. The award is to recognize the contribution and support to local law enforcement. He teaches his goalie school with Wild goaltending coach Bob Mason.
While with the Tampa Bay Lightning, Roloson wore a mask that had a shamrock with the initials "KR" to remember Kelly Ryan, a 12-year-old player who attended several of Roloson's goalie camps. The shamrock also had the letters "TDLO", "The Dream Lives On."