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O'Reilly enjoyed a career year in his first year in St. Louis, achieving career highs in assists and points and tying his career high in goals. For his excellent two-way play during the season, O'Reilly won the Frank J. Selke Trophy as the league's best defensive forward on April 17, 2019, over Patrice Bergeron and Mark Stone of the Boston Bruins and Vegas Golden Knights, respectively.

On June 12, 2019, O'Reilly and the Blues won their first Stanley Cup in franchise history, defeating the Boston Bruins 4–1 in game 7 of the 2019 Stanley Cup Finals. O'Reilly was awarded the Conn Smythe Trophy after recording a franchise-record 23 playoff points. O'Reilly became the first player to score a goal in four-consecutive Stanley Cup Finals games since Wayne Gretzky in 1985.

On April 7, 2018, O'Reilly surpassed Rod Brind'Amour for most faceoff wins in a single season (1,269) in a 4–3 loss to the Florida Panthers. At the end of the 2017–18 season, O'Reilly was named a Lady Byng Memorial Trophy finalist as the leagues most gentlemanly player.

On July 1, 2018, O'Reilly was traded to the St. Louis Blues in exchange for Tage Thompson, Vladimír Sobotka, Patrik Berglund, a 2019 first-round pick and a 2021 second-round pick.

O'Reilly repeated as World Champion with Canada in 2016. The following year, O'Reilly won silver at the 2017 IIHF World Championship. He was named an alternate captain for Team Canada at the 2018 IIHF World Championship.

On June 26, 2015, the Avalanche traded O'Reilly, alongside Jamie McGinn, to the Buffalo Sabres in exchange for Nikita Zadorov, forward Mikhail Grigorenko, prospect J. T. Compher and the 31st pick in the 2015 NHL Entry Draft. On July 2, O'Reilly then signed a seven-year contract extension with Buffalo worth $52.5 million, which came into effect during the 2016–17 season. O'Reilly's signing came on the same day as the Sabres organization signed his brother Cal O'Reilly to a two-year contract. O'Reilly was immediately named an alternate captain upon his arrival in Buffalo.

On July 13, 2015, Ontario Provincial Police charged O'Reilly with impaired driving following an incident in Lucan, Ontario when the pickup truck he was driving struck a Tim Hortons. He was charged with driving a motor vehicle while ability impaired and care or control over two bottles. He was acquitted of the charges on July 11, 2016.

As an impending restricted free agent, and with past difficulties in contract negotiation, the Avalanche elected to take O'Reilly to a salary arbitration. On July 23, 2014, O'Reilly and the Avalanche agreed to settle prior to the arbitration hearing after negotiating a two-year, $12 million contract. During the 2014–15 season, O'Reilly scored 17 goals and 38 assists for 55 points, also leading the Avalanche in average ice time per game, as Colorado failed to make the 2015 playoffs.

Unable to reach the playoffs with the Avalanche after the 2014–15 regular season, O'Reilly, for the third time in his professional career, was invited to participate in the 2015 IIHF World Championship in the Czech Republic. He helped contribute to a dominant Canadian team, scoring ten points in ten games as Canada won gold in the tournament final over Russia, their first victory in the World Championship since 2007.

Despite an end to NHL lock-out announced on January 12, 2013, O'Reilly was still unable to come to terms with the Avalanche and initially continued to play in Russia to miss the opening of the shortened 2012–13 season. On January 24, citing an ankle injury suffered through his 12 games with Metallurg, he mutually terminated his contract in Russia and returned for rehabilitation to North America. At an impasse with the Avalanche a month into the season, O'Reilly was training with the OHL's London Knights when he ended his holdout on February 28 after signing a two-year, $10 million offer sheet with the Calgary Flames. With a game coinciding between the two clubs on that day, the Avalanche announced during the contest that they opted to forgo compensation and secured O'Reilly to a contract by matching the Flames' offer sheet.

In the 2013–14 season, under new Head Coach Patrick Roy, O'Reilly was moved to the wing to play alongside centre Matt Duchene and subsequently responded with a team-leading—and career-high—28 goals and 64 points in 80 games as the Avalanche returned to the playoffs. For the second time in his career, O'Reilly led the NHL in takeaways with 83 and, in recording just one penalty minor, was awarded the Lady Byng Memorial Trophy for gentlemanly conduct and sportsmanship by the League.

In the following year, 2011–12, having established himself as the leading defensive centre on the Avalanche, O'Reilly developed his two-way game and increased his offensive production playing alongside linemate Gabriel Landeskog. This was recognized as he was named as the NHL's Second Star of the Week for November 28 to December 4 after contributing with seven points in four games, and was leading all Avalanche forwards in ice time. On January 12, 2012, he appeared in his 200th career NHL game, scoring a goal in a 3–2 overtime defeat to the Nashville Predators. Despite the Avalanche missing the playoffs for a second-straight season, O'Reilly lead the NHL and set an Avalanche record with 101 takeaways. He also more than doubled his points output for his previous two seasons combined to finish as top scorer on the Avalanche with 18 goals and 55 points.

As a restricted free agent in the off-season, O'Reilly's protracted contract negotiations with the Avalanche were halted by the expired Collective Bargaining Agreement between the NHL and the NHL Players' Association (NHLPA), which incurred the 2012–13 NHL lock-out. With the lock-out cancelling the start of the season, O'Reilly, in joining his brother Cal, signed a two-year contract with Russian Kontinental Hockey League (KHL) club Metallurg Magnitogorsk on December 7, 2012. Unlike the exodus of NHL players joining European leagues on short-term contracts, O'Reilly signed a two-year contract with the conditional opt-out clause in returning to the NHL if an agreement with the Avalanche was met. O'Reilly made his debut for Magnitogorsk in a 5–3 victory over Atlant Moscow Oblast on December 19.

Suffering an offensive plateau midway through the season, O'Reilly anchored his position as a top defensive forward and penalty killer. He led the Avalanche in ice time on the penalty kill, culminating in posting two short-handed goals during a double minor penalty against the Columbus Blue Jackets on February 2, 2010, to become the first Avalanche player in history to achieve two shorthanded goals in one game. He finished his rookie season with the Avalanche with 26 points (eight goals and 18 assists) in 81 regular season games before making his Stanley Cup playoff debut in a 2–1 victory over San Jose in Game 1 of the Western Conference Quarterfinals on April 14. On April 18, he scored his first career playoff goal, scoring the game-winning tally in Colorado's Game 3 1–0 overtime victory over San Jose. He was credited with the goal after inadvertently deflecting Sharks defenceman Dan Boyle's pass attempt from an improbable angle into the net past goaltender Evgeni Nabokov to put the Avalanche ahead in the series, two games to one.

In his second professional season in 2010–11, O'Reilly remained entrenched on the shut-down third line for the Avalanche. On November 19, 2010, he appeared in his 100th NHL game, a 5–1 victory over the New York Rangers. In scoring eight goals in his last 18 games, O'Reilly was able to match his rookie season contribution of 26 points and led the team for a second consecutive season in takeaways, with 72.

O'Reilly was drafted 33rd overall in the 2009 NHL Entry Draft by the Colorado Avalanche, with whom he spent the first six seasons of his NHL career. In 2015, O'Reilly was traded to the Buffalo Sabres, where he would play three seasons until being traded to the Blues in 2018. O'Reilly won the Stanley Cup with the Blues in 2019 over the Boston Bruins and was awarded the Conn Smythe Trophy as the most valuable player in the 2019 playoffs.

After the 2008–09 OHL season, O'Reilly was drafted in the second round, 33rd overall, in the 2009 NHL Entry Draft by the Colorado Avalanche. He became the youngest player in Avalanche history to appear in a regular season game when he surprisingly made the opening night roster for the 2009–10 season. He earned his first NHL point in his Avalanche debut on October 1, 2009, against the San Jose Sharks, becoming the first non-first-round draft pick to immediately make the NHL in his first post-draft year since Patrice Bergeron in 2003–04. O'Reilly later scored his first career NHL goal, a game-winner, on October 15 against Carey Price of the Montreal Canadiens. On October 19, following his strong start to the season, the Avalanche announced that O'Reilly and his fellow 2009 draftee Matt Duchene would spend the entire season with the Avalanche. Initially leading all rookie forwards in scoring through October, O'Reilly recorded an assist in a 3–1 victory over the Detroit Red Wings on October 24 to cap a seven-game point streak, which stood as the longest by a rookie throughout the season.

The following year, O'Reilly was selected as captain of Canada for the 2009 IIHF World U18 Championships. In six games, he contributed with five points before finishing in fourth place after losing 5–4 in the bronze medal game against Finland.

O'Reilly made his international debut at the 2008 World U-17 Hockey Challenge, scoring six points in six games as captain of gold medal-winning Team Ontario. As an underage 17-year-old, O'Reilly gained selection to Team Canada the 2008 Ivan Hlinka Memorial Tournament in Slovakia. He scored five points in four games and was named game MVP in the final against Russia as he helped Canada capture the gold medal for the fourth time in five years.

O'Reilly began playing at the major junior level for the Erie Otters of the Ontario Hockey League (OHL) after he was the recipient of the Jack Ferguson Award as the first overall selection in the 2007 OHL Draft. In his rookie season in 2007–08, O'Reilly put up a solid 52 points in 61 games and was named the Otters Rookie of the Year and Most Sportsmanlike Player while also earning Erie's nomination for the Bobby Smith Trophy. In the following year, he backed up his rookie year with 50 assists and 66 points in 68 games for the 2008–09 season, and his all-around game was noticed when he was named the Western Conference's best penalty killer.

O'Reilly grew up playing hockey near his hometown of Varna, Ontario, with the Seaforth Stars of the Ontario Minor Hockey Association (OMHA). He then moved up to the AAA level, playing for the Huron-Perth Lakers of the Minor Hockey Alliance starting in Minor Atom in 2000–01. Touted as one of the most talented prospects to come out from the Lakers, O'Reilly then played one year of minor midget hockey with the Toronto Jr. Canadiens in 2006–07 after playing six years of Lakers hockey.

Ryan O'Reilly (born February 7, 1991) is a Canadian professional ice hockey centre and alternate captain for the St. Louis Blues of the National Hockey League (NHL). He has previously played for the Colorado Avalanche and Buffalo Sabres.