Edmonton Oilers (2010–2015)

Upon completing what would be his final year at collegiate level, Petry signed a two-year, entry-level contract with the Edmonton Oilers on March 10, 2010.^[3] He was then briefly assigned to the Oilers' then-American Hockey League (AHL) affiliate, the Springfield Falcons, playing in eight games. He played his first game as a professional on March 26.

On September 30, 2010, Petry was assigned by the Oilers to their new AHL affiliate, the Oklahoma City Barons, for its inaugural season.^[4] On December 27, Edmonton recalled Petry from Oklahoma City. He then made his NHL debut against the Buffalo Sabres on December 28, 2010, and recorded his first NHL point, a secondary assist on a goal by Ryan Jones. His first NHL goal was scored on January 20, 2011, against Kari Lehtonen of the Dallas Stars. On February 4, 2011, Petry was reassigned back to the Barons.^[5]

Petry improved in his second NHL season, leading all Oilers defensemen in points, with 25, and was trusted into a shutdown role alongside Ladislav Šmíd.^[6] At the end of the 2011–12 season, on June 7, 2012, Petry re-signed on a two-year, $3.4 million contract with the Oilers.^[7]

At the start of the 2011–12 season, Petry made Edmonton's NHL roster out of training camp and subsequently played three regular season games before being assigned to Oklahoma City.^[8] After only two games in the AHL, however, Petry was recalled back to Edmonton, where he remained for the entire season, playing in 73 games.

After the Oilers missed the playoffs in 2012, Petry was invited to play for Team USA at the 2012 IIHF World Championship.^[9] He amassed six points in nine games, though the United States were eliminated in the quarter-finals by Finland.^[10] Petry stayed as a permanent member of the Oilers for the lockout-shortened 2012–13 season, playing in all 48 games as the Oilers again failed to make the Stanley Cup playoffs that year.

Montreal Canadiens (2015–2022)

On March 2, 2015, during the 2014–15 season, Petry was traded to the Montreal Canadiens in exchange for a 2015 second-round draft pick and conditional fifth-round pick.^[11] After the Canadiens post-season run, on June 2, 2015, Petry opted to surrender his impending free agent status in signing a six-year contract extension with the Montreal Canadiens until the 2020–21 season.^[12]

On September 25, 2020, Petry signed a four-year, $25 million contract extension with the Canadiens.^[13]

The 2020–21 COVID-shortened season proved to be Petry's most productive to date, while playing alongside Montreal newcomer Joel Edmundson.^[14] His 42 points over 55 games was second on the team, behind only Tyler Toffoli. Petry participated in the Canadiens' deep run during the 2021 Stanley Cup playoffs, culminating in an appearance in the 2021 Stanley Cup Finals, where they lost to the Tampa Bay Lightning in five games. Petry sustained a finger injury in the course of Game 3 of the second round series against the Winnipeg Jets, causing him to miss two games. He opted against surgery to remain in the series, instead having it put in a cast, the pain from which caused blood vessels in both his eyes to pop, and he returned to Game 2 of the semi-final against the Vegas Golden Knights with noticeably bloodshot eyes that became an internet meme.^[15]

With Shea Weber's departure from the lineup for health reasons, Petry became the Canadiens' top defenseman going into the 2021–22 season.^[14] Expectations were high based on four consecutive forty point seasons, but Petry's struggles became one of the most prominent features of a historically poor start for the team. In his first 25 games, Petry recorded only 2 secondary assists, and committed numerous miscues that attracted commentator and fan speculation that he was attempting to play through injury. His poor play lead fans of the team to derisively dub him the "Tank Commander".^[16] In December, shortly after the sacking of longtime general manager Marc Bergevin, the team announced that Petry was dealing with an upper body injury and would miss an undetermined number of upcoming games.^[17] The change in management with the hiring of Jeff Gorton and possibility of the Canadiens initiating a long-term rebuild raised questions about whether Petry would seek a trade. He said "when you get later in your career — as a I am — you know time’s not on your side. So that’s a decision that they need to make and to be aware of what they’re going to do."^[18] Petry was vocally critical of coach Dominique Ducharme.^[19] His situation became more complicated still when his wife Julie became frustrated with the Quebec government's pandemic measures and relocated with their children to Detroit for the remainder of the season.^[20]

Following Ducharme's sacking by new general manager Kent Hughes and the hiring of Martin St. Louis to replace him, Petry's play markedly improved.^[19] However, he remained interested in a trade for family reasons. Hughes attempted to facilitate one at the trade deadline, but none took shape, and he said that he would attempt again in the summer.^[20] Petry subsequently sustained a lower body injury in a March 24 game against the Florida Panthers, exiting in the third period, and was announced as being out indefinitely.^[21] After returning, he played what was widely judged as his best hockey of the season in the final weeks of April, including a two-goal performance to help the team beat the New York Rangers 4–3, snapping a nine-game losing streak in the penultimate game of the year.^[16]

Pittsburgh Penguins (2022–2023)

On July 16, 2022, Petry, along with forward Ryan Poehling, was traded to the Pittsburgh Penguins in exchange for Mike Matheson and a 2023 fourth-round draft pick.^[22] Having been acquired by general manager Ron Hextall in the hopes that he would improve the offensive performance of the Penguins' blueline, there was a general sense of disappointment with Petry's first season with the team, despite generating 31 points in 61 games. He missed time with injury, and in the midst of an underwhelming season for the Penguins that saw them miss the playoffs for the first time in 17 years, there were reports that new general manager Kyle Dubas was looking to trade Petry elsewhere.^{[23][24][25][26]}

Detroit Red Wings (2023–present)

On August 6, 2023, Petry, alongside Casey DeSmith, Nathan Legare, and a 2025 second-round pick, was traded back to Montreal in exchange for Rem Pitlick and Mike Hoffman as part of a three-team trade also involving the San Jose Sharks.^[27] It was widely speculated that general manager Hughes would seek to immediately trade Petry to another team; as a result, Petry was again traded to the Detroit Red Wings in exchange for Gustav Lindström and a conditional 2025 fourth-round pick on August 15.^{[28][29][30][31]}