Werenski helped Team USA win gold at the Olympic Winter Games Milano Cortina 2026 with his assist on Jack Hughes' goal in a 2-1 overtime victory against Team Canada that gave the U.S. its first gold medal in men's Olympic hockey since the 1980 Lake Placid Games. He represented the United States at the IIHF World Junior Championship in 2015 and '16, was team captain when it won bronze in 2016 and helped the U.S. to gold at the 2025 IIHF World Championship, its first at Worlds since 1933.

He finished the regular season second among NHL defensemen with 81 points (22 goals, 59 assists) in 75 games to become a finalist for the 2026 Norris Trophy given to the best player at his position. Werenski also led defensemen in shots on goal (260) and his 1.08 points per game were second at the position behind Evan Bouchard of the Edmonton Oilers (1.16).

Werenski was a 2025 Norris finalist after finishing second among defensemen behind Cale Makar of the Colorado Avalanche with 82 points (23 goals, 59 assists). He set Blue Jackets single-season records at the position in all three categories, and average ice time, an NHL-best 26:45. He also was third among all skaters with 298 shots on goal and is the ninth defensemen since 1997 to finish a season with at least 80 points.

After scoring 25 points (nine goals, 16 assists) in 35 games as a freshman at the University of Michigan, Werenski was selected by the Blue Jackets with the No. 8 pick in the 2015 NHL Draft. He followed that with 36 points (11 goals, 25 assists) in 36 games as a sophomore, earning All-Big Ten First Team honors again, and was named Big Ten Defensive Player of the Year. He ranked second among defensemen in NCAA Division I with 36 points, and he was named an AHCA First Team All-American.

Soon after finishing his sophomore season at Michigan, Werenski signed a three-year, entry-level contract with the Blue Jackets on March 29, 2016.

Werenski emerged for Lake Erie of the American Hockey League in the 2016 Calder Cup Playoffs with 14 points (five goals, nine assists) in 17 games to help win the championship. He started the 2016-17 season with the Blue Jackets and made his NHL debut against the Boston Bruins on Oct. 13, 2016 and got an assist for his first NHL point. He scored his first NHL goal in his second game two days later, against the San Jose Sharks in Columbus. Werenski finished third that season for the Calder Trophy, awarded to the League's top rookie, after getting 47 points (11 goals, 36 assists) in 78 games.

Werenski played all 82 regular-season games in 2018-19 and scored 44 points (11 goals, 33 assists). He helped the Blue Jackets win a Stanley Cup Playoff series for the first time, a four-game sweep of the Tampa Bay Lightning in the Eastern Conference First Round. He finished with six points (one goal, five assists) in 10 playoff games.

A restricted free agent after that season, Werenski signed a three-year, $15 million contract with the Blue Jackets on Sept. 9, 2019. He had 41 points, including an NHL career high 20 goals, when the NHL season was paused March 12, 2020, due to concerns surrounding the coronavirus.