He likewise held the position of assistant coach roles with the Coyotes, Vancouver Canucks, Tampa Bay Lightning and Stars.

Bowness spent the majority of his first professional season in 1975–76 with the Tulsa Oilers of the Central Hockey League (CHL), where in 64 games, he earned 25 goals and 63 points, and had 160 penalty minutes.

Bowness also played two games with Nova Scotia Voyageurs of American Hockey League (AHL), recording one assist.

Bowness also made his National Hockey League(NHL) debut during the 1975–76 season, going pointless in five games with the Atlanta Flames.

In four playoff games with Detroit, Bowness was held off the scoresheet as the Red Wings lost to the Montreal Canadiens in the quarter-finals.

He was set to return to the Red Wings for the 1978–79 season, however, on October 10, 1978, Detroit traded Bowness to the St. Louis Blues for cash.

In 71 games with Salt Lake, Bowness had 25 goals and 71 points to finish fifth in team scoring, while accumulating a team-high 135 penalty minutes.

He spent the entire 1981–82 regular season playing with Tulsa, finishing second on the team in scoring with 34 goals and 87 points in 79 games.

Bowness led the expansion team to a 27–43–8–2 record, earning 64 points and a sixth-place finish in the North Division, failing to qualify for the playoffs.

Bowness coached his first NHL game on February 9, 1989, as the Jets lost to the New York Rangers 4–3 at Madison Square Garden.

After a 0–3–1 start, Bowness earned his first NHL victory on February 17, 1989, defeating the New Jersey Devils 3–2 in overtime at the Winnipeg Arena.

The Bruins eventually won the series in seven games, followed by a four-game sweep over the Montreal Canadiens to reach the Wales Conference finals.

On October 8, 1992, the Senators won the franchise's first game, over the eventual Stanley Cup champion Montreal Canadiens 5–3 at the Ottawa Civic Centre.

With a lineup perilously thin on talent, wins for Bowness and the Senators were few and far between, and Ottawa finished with a league-worst 10–70–4 record, earning 24 points and a tie for last place in the overall NHL standings with the San Jose Sharks.

Bowness returned as the Islanders' head coach for the 1997–98 season; however, the club struggled to a 22–32–9 record, and he was fired, as Mike Milbury replaced him behind the bench.

Bowness joined the Phoenix Coyotes (the former Winnipeg Jets) coaching staff as an assistant under Bobby Francis for the 1999–2000 season.

The club had another tough season in 2003–04, as the Coyotes had a 20–24–15–3 before the team fired Francis and named Bowness as interim head coach.

With the 2004–05 NHL lockout cancelling the season, Bowness returned to the club in 2005–06 as an assistant under new head coach Wayne Gretzky.

Vancouver rebounded in 2008–09, winning the Northwest Division for the second time in three seasons, going 45–27–10, recording 100 points and third place in the Western Conference.

The 2009–10 was another very successful season for the Canucks, as the club once again won the Northwest Division with a 49–28–5 record, good for 103 points and third in the Western Conference.

In the postseason, Vancouver defeated their rivals, the defending Stanley Cup champion and eighth-seeded Chicago Blackhawks in seven games, followed by winning a six-game series against the fifth-seeded Nashville Predators to make the Western Conference final for the first time since 1994.

The Canucks easily defeated the second seeded San Jose Sharks in five games to clinch a berth in the 2011 Stanley Cup Finals against the third-seeded Boston Bruins.

[3] Despite this, the Canucks would get defeated in five games in the first round of the 2012 playoffs by the eighth-seeded and eventual Stanley Cup champion Los Angeles Kings.

[11] He was dismissed on May 31, 2018, after general manager Steve Yzerman called the defense "not quite good enough" during the 2017–18 regular season where the Lightning finished as the top seed in the Eastern Conference and the 2018 playoffs which saw the Lightning reach the Eastern Conference Finals and losing in seven games to the second-seeded and eventual Stanley Cup champion Washington Capitals, one win short from the Stanley Cup Finals once more.

[13][14] On December 10, 2019, he was named interim head coach of the Stars after Jim Montgomery was fired due to unprofessional conduct.

[18] After a disappointing COVID-19-shortened 2020–21 campaign, Bowness guided the Stars back to the postseason in 2022 where they lost a close seven-game series to the Calgary Flames.

[19][20] On July 3, 2022, the modern Winnipeg Jets franchise named Bowness head coach, replacing Dave Lowry.

[21] During the 2023–24 season, he spent time away from the team twice, first because of a seizure his wife experienced in October 2023, and then for a minor medical procedure of his own in March 2024.