In 2001, Perry led his Petes to a victory in the inaugural OHL Cup Bantam AAA championship held in Peterborough.

In the playoffs, Perry scored no goals but managed three assists as the Ducks were eliminated in the Western Conference Final to the eighth seeded Edmonton Oilers.

In 2006–07, his sophomore season, Perry improved to 44 points (17 goals, 27 assists) in all 82 games, playing with Ryan Getzlaf and Dustin Penner on a combination dubbed the "Kid Line".

[18] His goals came at even strength, shorthanded and on the power play, making him the second player in Ducks history to score in all three situations, the other being Paul Kariya.

From March 19 through April 6, Perry recorded a least a point in ten consecutive games, later taking the NHL scoring lead from Tampa Bay Lightning forward Steven Stamkos when he scored two goals in a 2–1 win against the Chicago Blackhawks on Blackhawks' goaltender Corey Crawford on March 26.

[23] Despite managing to score 37 goals, 23 assists and 60 points, the Ducks missed the 2012 playoffs after finishing fifth in the Pacific Division and 13th in the Western Conference.

Perry's 2013–14 season turned out to be one of his best as he had 43 goals, 39 assists and 82 points in 81 games played, helping the Ducks win their second consecutive Pacific Division title and was the runner up for the Rocket Richard Trophy only behind Washington Capitals forward and captain Alexander Ovechkin who ended with a league leading 51 goals.

On June 19, 2019, Perry's 14-year tenure with the Ducks ended after he was bought-out from the remaining two years of his eight-year contract to become an unrestricted free agent.

[citation needed] On July 1, 2019, Perry signed on the opening day of free agency to a bonus laden one-year, $1.5 million contract with the Dallas Stars.

[31] During the 2020 Bridgestone NHL Winter Classic on January 1, 2020, Perry was issued a game misconduct for elbowing Nashville Predators defenseman Ryan Ellis at 2:40 of the first period.

[33] The Stars were on a six-game losing streak when the season ended, but when the NHL later scheduled the 2020 playoffs to take place in late summer in a bubble environment in Edmonton, things proved to be different.

[34] He went on to contribute to the team's second round win over the Colorado Avalanche, and provided the screen for Denis Gurianov's Western Conference Final-clinching goal against the Vegas Golden Knights.

[35] On December 28, 2020, Perry extended his career by signing as a free agent to a one-year, $750,000 contract with the Montreal Canadiens.

[40][41] The Canadiens qualified for the fourth berth in the North Division in the 2021 playoffs, entering a first round matchup with the Toronto Maple Leafs as decided underdogs.

I know Johnny pretty well and just hope he’s OK."[45][46] On reaching the 2021 Stanley Cup Finals, his second consecutive with two different clubs and third overall appearance, Perry reflected that "you come into this League at a young age, and you have success early.

The Canadiens were ultimately defeated in five games as the Lightning won their second straight Stanley Cup title.

[49] However, General Manager Marc Bergevin declined to offer Perry a two-year contract, and he opted to sign elsewhere.

[50][29] On July 29, 2021, Perry, having played in two consecutive Stanley Cup Finals losing efforts against the Tampa Bay Lightning, opted to join the back-to-back champions on a two-year, $2 million contract.

[54] The two time defending Stanley Cup Lightning qualified for the 2022 playoffs as they finished the season as the fifth seed in the Eastern Conference, and for the second consecutive year, Perry faced the Maple Leafs in the first round, again beating them in seven games.

Perry became only the second player in the history of the NHL to go to the Finals in three consecutive years with three different teams, after Marián Hossa.

On June 29, 2023, Tampa Bay traded the negotiation rights for Perry to the Chicago Blackhawks in exchange for a 2024 seventh-round pick.

[59] On November 25, after he had been a healthy scratch for the Blackhawks' last two games, the team announced Perry would take an indefinite leave of absence for personal reasons.

[60] On November 28, the Blackhawks placed Perry on unconditional waivers, stating that an internal investigation revealed that he had "engaged in conduct that is unacceptable, and in violation both of the terms of his Standard Player's Contract and the Blackhawks' internal policies intended to promote professional and safe work environments."

[61][62] At a press conference on November 28, Davidson said that the Blackhawks had learned of misconduct on Perry's part while the team was preparing to play against the Columbus Blue Jackets.

According to Davidson, when team officials learned this information, they pulled Perry from the lineup and began an internal investigation, which culminated in the decision to cut ties with him.

[67] On April 16, 2010, Perry was among the first group of 15 players to be named to Canada for participation at the 2010 IIHF World Championships in Cologne, Mannheim and Gelsenkirchen, Germany.

In Canada's first game of the 2010 Winter Olympics, Perry helped lead the team to an 8–0 victory over Norway, scoring one goal.

Perry contributed one assist in Canada's six games en route to a gold medal victory at the 2014 Winter Olympics over Sweden in Sochi.

At the 2016 IIHF World Championship, Perry served as captain en route to a gold medal finish.

Perry's younger brother Adam played alongside him on the London Knights' 2005 Memorial Cup-winning team.