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On June 21, 2017, Merrill was selected in the NHL Expansion Draft by the Vegas Golden Knights. On January 16, 2018, Merrill signed a two-year, $2.75 million contract extension with the Golden Knights.

He scored his first NHL goal on February 7, 2014, a game winner in overtime against Ilya Bryzgalov of the Edmonton Oilers, making him the first Devil to score his first NHL goal in overtime.

On March 27, 2013, the New Jersey Devils signed Merrill to a three-year entry-level contract, and he began the 2013–14 season in the American Hockey League (AHL) with the Albany Devils.

In the 2013–14 season, Merrill made his NHL debut on November 3, 2013, skating with the Devils in a game against the Minnesota Wild at Xcel Energy Center, but less than five minutes into he game he fell into the boards, sustaining severe facial lacerations and a concussion.

Prior to turning professional, Merrill played NCAA college hockey with the Michigan Wolverines men's ice hockey team. Merrill was suspended for the first 12 games of the 2011–12 season by the University of Michigan for "violating team rules."

As a youth, Merrill played in the 2004 Quebec International Pee-Wee Hockey Tournament with the Detroit Little Caesars minor ice hockey team.

Jonathon Merrill (born February 3, 1992) is an American professional ice hockey defenseman for the Vegas Golden Knights of the National Hockey League (NHL). Merrill was selected by the New Jersey Devils in the 2nd round (38th overall) of the 2010 NHL Entry Draft. Merrill was born in Oklahoma City, Oklahoma, but grew up in Grand Blanc, Michigan and Brighton, Michigan.