On June 25, 2016, the Tampa Bay Lightning selected Howden with the 27th overall pick in the 2016 NHL entry draft. In the season leading up to the NHL draft, Howden recorded 24 goals and 40 assists over 68 games with the Moose Jaw Warriors of the Western Hockey League (WHL). Howden finished fourth on the team in goals and points, and also added four goals and 11 assists in 15 postseason games, which included four-straight multi-point games in the first round against the Prince Albert Raiders. In addition, Howden was named the Warriors' Rookie of the Year and Most Sportsmanlike Player during his rookie year in 2014–15. Howden has played two seasons with Lightning forward Brayden Point. Howden said that the team's familiarity with Point and their scouting of Moose Jaw played a role in their decision to select him. The team had spoken to Point about Howden leading up to the 2016 draft.[1]
On September 30, 2016, the Warriors named Howden the 31st captain in team history.[2] Howden previously served as alternate captain the previous season as a 17-year-old, and had also served as captain of Canada under-18 team, leading the team to a gold medal during the 2015 Ivan Hlinka Memorial Tournament.[2] Howden credited former Warriors captain, Point, with his growth as a leader on the team.[2]
On December 28, 2016, Howden signed a three-year, entry-level contract with the Tampa Bay Lightning.[3]
On November 22, 2024, during the 2024–25 season, and as a pending free agent, Howden signed a five-year extension with the Golden Knights, keeping him in Vegas through the 2029–30 season.[11]
On November 29, 2016, Howden was announced as one of the Canada junior team invitees for the 2016 World Junior Championships training camp where Howden was joined by five other Lightning prospects.[13] On December 13, 2016, Howden was released from the training camp as part of the initial roster cuts.[14]