Pionk was signed by the New York Rangers as an undrafted college free agent May 1, 2017, after his sophomore season at the University of Minnesota Duluth, where he finished fifth among NCAA defensemen in scoring with 34 points (seven goals, 27 assists). That season, the Bulldogs advanced the NCAA championship game before losing to the University of Denver.

He chose to attend UMD after playing two seasons with Sioux City of the United States Hockey League. In 2014-15, he led all USHL defenseman with 48 points (seven goals, 41 assists) in 53 games and won the USHL Defenseman of the Year Award.

In the 2017-18 season, Pionk played 48 games with Hartford of the American Hockey League before being called up by the Rangers on Feb. 8, 2018. He made his NHL debut the following night against the Calgary Flames and scored his first NHL goal against the Buffalo Sabres on March 24, 2018 . He finished with 14 points (one goal, 13 assists) in 28 games with New York.

On April 28, 2018, Pionk played for the United States at the 2018 IIHF World Championship. He had three points (two goals, one assist) in 10 games to help the U.S. finish third.

Pionk had 26 points (six goals, 20 assists) in 73 games for the Rangers in 2018-19, then was traded to the Winnipeg Jets on June 17, 2019, with a first-round pick in the 2019 NHL Draft for defenseman Jacob Trouba. He signed a four-year, $23.5 million contract with the Jets on Aug. 11, 2021, to avoid a salary arbitration hearing and received a six-year, $42 million contract April 17, 2025, beginning with the 2025-26 season. His average ice time of 22:04 was second on the Jets and he tied for third with a plus-21 rating in 2024-25.

Pionk's shot was deflected by Jets captain Adam Lowry past St. Louis Blues goalie Jordan Binnington to give Winnipeg a 4-3 win in double overtime in Game 7 of the 2025 Western Conference First Round at Canada Life Centre. He became the fifth defenseman in NHL history with three assists in a Game 7, joining Jaccob Slavin of the Carolina Hurricanes (2019 first round), Brian Rafalski of the Detroit Red Wings (2010 conference quarterfinals), James Patrick of the New York Rangers (1992 Patrick Division Semifinals) and Paul Reinhart of the Calgary Flames (1981 quarterfinals).