Merkley was selected ninth overall by the
Kelowna Rockets in the 2012 WHL Bantam Draft. Following a strong first season with the Rockets, he was selected as the
2013–14 WHL Rookie of the Year and awarded the
Jim Piggott Memorial Trophy, and during the
2014–15 WHL season he was rewarded for his outstanding play when he was selected to skate in the 2015
CHL/NHL Top Prospects Game and was also named to the
2014–15 WHL (West) Second All-Star Team after scoring 20 goals and 90 points in 72 games. On September 3, 2015, Merkley agreed to a three-year entry-level contract with the Arizona Coyotes. He made his NHL debut on December 19, 2017, against the
Florida Panthers. He played 13 minutes 30 seconds of ice time in a 3–2 loss. He was sent back down to the AHL shortly after. On January 4, 2018, Merkley was selected for the 2018 AHL All-Star Classic Game in Utica, New York. During the
2019–20 season while with the Tucson Roadrunners, Merkley was traded by the Coyotes to the New Jersey Devils in a deal involving star forward
Taylor Hall on December 16, 2019. Merkley joined the Devils' AHL affiliate, the
Binghamton Devils, and was instantly productive in collecting 8 goals and 19 points in 28 regular season games. He was later recalled by the New Jersey Devils, adding a goal and an assist in four games, before the regular season was abruptly ended due to the
COVID-19 pandemic. As an impending restricted free agent with the Devils and with the team unable to qualify in the return to play format, Merkley signed a one-year contract with the Finnish
Liiga club
Ässät on August 27, 2020, in order to stay in game shape. His contract included an NHL-out clause until commencement of the delayed 2020–21 North American season. On July 26, 2021, Merkley was traded to the
San Jose Sharks in exchange for
Christián Jaroš. He signed a one-year contract three days later. He made his debut for the Sharks on October 30, 2021, in a 2–1 win over the
Winnipeg Jets. Three days later, he recorded his first point as an assist in a 5–3 victory against the
Buffalo Sabres. His first goal came on November 4, 2021, in a 3–5 loss to the
St. Louis Blues. On March 21, 2022, Merkley was traded by the Sharks to the
New York Rangers in exchange for
Anthony Bitetto at the NHL trade deadline. On August 1, 2022, having left the Rangers as a free agent, Merkley agreed to a one-year contract with Belarusian club, HC Dinamo Minsk of the KHL, for the
2022–23 season. On July 8, 2024, Merkley signed a two-year contract to play for another KHL team,
Avtomobilist Yekaterinburg. On 16 August 2025, Merkely continued his career in the KHL, moving to newly rebranded Shanghai Dragons on a one-year contract for the
2025–26 season. ==International play==