[3] Marner played his minor career in the Durham Region and the Greater Toronto Hockey League (GTHL).

[4] For the 2012–13 season, Marner transitioned to the Don Mills Flyers of the GTHL, where he played his minor midget year, registering 86 points in 55 games.

At the end of his season with the Flyers, Marner was immediately invited to join the St. Michael's Buzzers of the Ontario Junior A Hockey League, where he went on to win a championship.

He received a scholarship offer from the University of Michigan to play for the Wolverines ice hockey team, while also being drafted by the London Knights in the first round of the 2013 OHL Priority Selection, 19th overall.

[10] Marner played an important role during the Knights' 2016 playoff run, resulting in the team winning the OHL Championship.

[13] After an impressive training camp and pre-season (in which he led the team with four assists), it was announced that Marner would remain on the Toronto Maple Leafs roster for the upcoming 2016–17 season.

[22][23] Marner spent the entire season on a line with Van Riemsdyk and Tyler Bozak, finding offensive chemistry with the two veterans, and managed to finish the year with 61 points.

[24] The trio of Marner, William Nylander, and Auston Matthews became only the second team since the 1981 Quebec Nordiques to have three rookies finish with at least 60 points.

[31] On October 27, Marner recorded his 100th career assist on a game-tying goal by Jake Gardiner against the Winnipeg Jets to help the Leafs win 3–2.

[34] On January 17, 2019, Marner recorded a goal during a 4–2 win over the league-leading Tampa Bay Lightning, becoming the first player in Maple Leafs franchise history to begin his NHL career with three consecutive 60-point seasons.

[38][39] On November 9, 2019, during a game against the Philadelphia Flyers, Marner fell awkwardly onto his leg and was expected to miss a minimum 4 weeks due to an ankle injury.

Down 6–4 in the 3rd period, Marner sparked the Leafs comeback when he one-timed a spinning cross-ice pass from Auston Matthews to cut the Hurricanes lead.

[41] On February 7, 2020, Marner recorded his 200th NHL assist on a late overtime goal scored by John Tavares in a 5–4 win over the Anaheim Ducks.

Months later, the NHL arranged to hold the 2020 Stanley Cup playoffs in a bubble, with Eastern Conference games held in Toronto.

[49] On February 26, 2022, Marner recorded a career high four goals and six points to help the Toronto Maple Leafs to a 10-7 win over the Detroit Red Wings.

[50] Having accrued 97 points, Marner hoped to become only the fourth Maple Leaf player to break the 100-point barrier, but coach Sheldon Keefe opted to sit him out of the final game of the season to prepare for the playoffs.

[52] Advancing into the Stanley Cup playoffs, Marner and the Maple Leafs drew the Tampa Bay Lightning, two-time defending champions, in the first round.

[49] Marner had not scored a goal in eighteen playoff games prior to the beginning of the series, and in light of disappointing results against both the Blue Jackets and the Canadiens, how he would perform against the Lightning was subject to considerable speculation.

He was one of only twelve players in NHL history to record a streak of at least that many games, noting that it was "a cool accomplishment to have your name with some great legends.

While the Leafs were generally identified as the favourites going into the series, the long history of failure to advance past the first round was widely acknowledged.

[60][61][62] Many suggested that the outcome of the series would have major ramifications for the team going forward, including the status of both general manager Kyle Dubas and head coach Keefe, and also for the prospect of Matthews re-signing in Toronto, which he would become eligible to do in the summer.

After putting up 76 points in the 2023–24 season Marner suffered a high ankle sprain in a March 7 game against the Boston Bruins.

During a game against the Boston Bruins on January 4, 2025, Marner factored on a game-opening goal for the 112th time in his career, surpassing former captain Doug Gilmour and tying Börje Salming for the fifth most by a player in Maple Leafs history.

Marner made his international debut for Canada at the 2014 Ivan Hlinka Memorial Tournament, where he won a gold medal.

In July, 2020, Marner became part owner of OverActive Media, an esports company with Call of Duty and Overwatch teams based in Toronto.