Monahan played with the Mississauga Rebels. As a 15-year-old in 2010, he captained the Rebels to an OHL Cup title and was named most valuable player of the tournament. He finished the 2009–10 season with 46 goals and 40 assists in 47 games for the Rebels and was then selected by the Ottawa 67’s in the first round, 16th overall, at the Ontario Hockey League (OHL) Priority Selection draft. Monahan’s junior hockey career began with difficulty as he suffered a sprained wrist in his first training camp with the 67’s, resulting in a slow start for him in the 2010–11 OHL season. An invitation to play in the 2011 World U-17 Hockey Challenge, in which he was a key performer for the gold medal-winning Team Ontario, allowed Monahan to regain confidence; he completed his first OHL season on the 67’s second line and recorded 47 points in 65 games. Monahan played in his second international tournament following the season. He joined the Canadian Under-18 National Team for the 2011 Ivan Hlinka Memorial Tournament and scored a goal in the championship game to help Canada win a fourth consecutive gold medal at the event.

Monahan was one of the top-ranked prospects for the 2013 NHL Entry Draft: The NHL Central Scouting Bureau ranked him as the 5th best North American skater in its final ranking while International Scouting Services ranked him 9th overall. Among OHL draft prospects, the league’s coaches rated Monahan highly for his intelligence on the ice, playmaking and stickhandling, and for his faceoff ability. He was selected in the first round, sixth overall, by the Calgary Flames. Upon his selection, the 18-year-old centre expressed his confidence that he was ready to immediately play in the NHL. He earned a spot on the Flames roster to begin the 2013–14 season and made his NHL debut on October 3, 2013, against the Washington Capitals. Monahan scored his first career point in the game, assisting on David Jones’ goal in a 5–4 shootout loss. He then scored his first goal the following night against goaltender Sergei Bobrovsky of the Columbus Blue Jackets in a 4–3 win.

On August 19, 2016, following back-to-back seasons in which he scored 60 or more points, Monahan, as a restricted free agent signed a seven-year, $44.625 million contract extension to remain in the Flames’ organization through 2023.

On November 18, 2017, in a game against the Philadelphia Flyers, Monahan scored his first career hat trick in the second period to help the Flames win 5–4. However, his season was cut short in March due to injuries. During the following month, Monahan underwent four surgeries but was expected to be able to play during the 2018–19 season.

Monahan scored his 100th career goal against Andrei Vasilevskiy of the Tampa Bay Lightning on February 23, 2017. He is the 6th youngest active player to achieve this milestone, joining the elite company of Alexander Ovechkin, Sidney Crosby, Jaromír Jágr, Steven Stamkos, and Patrick Kane. His 100th goal also marked his 20th of the season, marking the 4 consecutive season he has scored at least 20 goals.

He became the fastest player in the Flames’ franchise to record 9 career overtime goals when he scored his 9th on December 7, 2017 vs the Montreal Canadiens in a 3-2 win.