He played 19 seasons in the National Hockey League (NHL) for the Detroit Red Wings, St. Louis Blues, Boston Bruins, Washington Capitals, Philadelphia Flyers, Mighty Ducks of Anaheim and Edmonton Oilers from 1985 to 2004.

[6] As the league's leading scorer, he won the Bobby Allan Award and in one game that season, set OLA Junior A single-game records of 19 assists and 29 points.

[4] Oates played one season of Senior A with the Brampton Excelsiors of Major Series Lacrosse but left the game in 1984 to focus on his hockey career.

[7] RPI's assistant coach Paul Allen noticed Oates during a 1982 OPJAHL game while scouting a different player and offered him a position on the school's team.

[11] After scoring 42 points in 22 games in his freshman season of 1982–83,[8] he spent the summer working with a skating instructor to improve his foot speed.

[13] He was inducted into RPI's Athletics Hall of Fame and was named the inaugural member of the hockey team's Ring of Honor in 2004.

[7] Choosing to forgo his final year of college eligibility, Oates signed a four-year, $1.1 million contract with the Detroit Red Wings that made him the highest paid rookie in the NHL in 1985–86.

[15] He made his NHL debut on October 10, 1985, against the Minnesota North Stars, scoring his first goal that night on goaltender Don Beaupre and added an assist.

[16] After this, Oates struggled offensively and was pointless in his following 16 games; the team subsequently demoted him to the Adirondack Red Wings of the American Hockey League (AHL).

[8] Having finished the NHL season in Detroit, he was returned to Adirondack for the AHL playoffs, which the team won to take the Calder Cup championship.

[19] However, Detroit made changes following a first round loss in the playoffs;[20] Oates, along with Paul MacLean, was traded to the St. Louis Blues on June 15, 1989, in exchange for veterans Bernie Federko and Tony McKegney.

[21] The deal, which is now considered one of the worst in Red Wings' history, left Oates "heartbroken" to leave his first NHL club.

[27] In game five of the conference quarter-final series against the New Jersey Devils, Oates scored the final goal in the history of the Boston Garden in a 3–2 loss.

The Bruins signed him to a five-year, $10 million contract extension late in that season,[30] but Oates once again became frustrated with his salary relative to the rest of the league by 1997.

In the trade, Oates, Bill Ranford and Rick Tocchet went to Washington in exchange for Jim Carey, Anson Carter, Jason Allison and two draft picks, 3rd Round 1997 (Lee Goren) & Conditional 2nd Round 1998 (Bobby Allen) [32][8] Oates initially refused to report to Washington, demanding his contract be renegotiated, but chose to join the team after a four-day holdout.

[34] After several months of contentious negotiations, the two sides agreed to a three-year contract worth around $2.9 million per season with an option on a fourth year.

[37] The Capitals named Oates the ninth captain in franchise history prior to the 1999–2000 season, following the departure of his predecessor, Dale Hunter.

[27] On January 14, 2002, Oates became the eighth player in NHL history to reach 1,000 career assists when he set up Dainus Zubrus' overtime winning goal in a 1–0 victory over the Boston Bruins.

[27] Anaheim reached the 2003 Stanley Cup Finals, where in the third game of the series against the New Jersey Devils, Oates assisted on Ruslan Salei's overtime-winning goal.

It was Oates' ninth career playoff overtime point, tying him with Joe Sakic and Doug Gilmour for the NHL all-time lead.

Oates was one of the NHL's great playmakers, a style that he credits his father as encouraging: "It was just kind of our family talks: 'If you can be unselfish, your teammates will always like you.'

He is also the only player in NHL history to centre three 50-goal scorers, helping Brett Hull, Cam Neely, and Peter Bondra reach the mark.

[47] His teammates praised his consistency, noting Oates continued to score points at an elite level when he did not have star players as linemates.

[53] Oates then joined the New Jersey Devils in 2010, where he served an additional two years as an assistant coach, helping the team reach the 2012 Stanley Cup Finals, which they lost to the Los Angeles Kings in six games.

"[54] The same day Oates was elected to the Hockey Hall of Fame, June 26, 2012, he returned to Washington Capitals, where he was named the 16th head coach in franchise history, succeeding Dale Hunter, who had decided not to renew his contract.

[56] While the 2012–13 NHL lockout delayed Oates' debut with the Capitals, he acted as co-coach with Mark French for Washington's AHL affiliate, the Hershey Bears.

[58] Oates' players praised his positive outlook and willingness to work closely with them as primary reasons why the team was able to turn its season around.

As a consequence, the Capitals opted to dismiss both Oates as head coach and the team's general manager, George McPhee.

[63] Oates and Stevens were assisted by Devils general manager Lou Lamoriello, who had previously served as the team's interim head coach.

[28] Oates is a co-founder of sporting apparel retailer Old Time Hockey, which donates a portion of all sales to the NHL emergency assistance fund.