As a true freshman at Missouri in 2018, he played in all 13 games recording 22 tackles and one sack. As a sophomore in 2019, he became a starter.[5][6][7] He had two interceptions, including one for a touchdown, in a game against West Virginia in the 2019 season.[8] He was named first-team All-Southeastern Conference (SEC) after finishing with 103 tackles, two interceptions and one sack.[9] During a COVID-19 scheduled ten game season in 2020, Bolton finished with 95 tackles and two sacks to close out his junior year.[10] He was once again named first-team All-SEC. In addition, he received Associated Press Second-team All-American honors.[11]
Bolton was selected by the Kansas City Chiefs in the second round (58th overall) of the 2021 NFL draft. The Chiefs used a 2nd round selection they previously acquired along with Orlando Brown Jr. in a trade that sent the 31st overall pick in the 2021 NFL draft (Odafe Oweh) to the Baltimore Ravens.[14] On May 13, 2021, Bolton officially signed with the Chiefs on a $5.84 million deal.[15]
Bolton was put on the Reserve/COVID-19 list on December 21, 2021.[16] He was activated on December 25, 2021.[17] In Week 18, against the Denver Broncos, he recorded his first NFL touchdown on an 86-yard fumble return in the 28–24 victory.[18] As a rookie, he appeared in 16 games and started 12. He finished with 112 total tackles and three passes defended.[19] He was named to the 2021 PFWA All-Rookie Team.[20]
During the 2022 season, Bolton recorded two sacks, 180 total tackles (108 solo), two interceptions, three passes defended, and one forced fumble.[21] He finished second in the NFL in combined and solo tackles in the 2022 season.[22] Bolton helped the Chiefs reach Super Bowl LVII where they defeated the Philadelphia Eagles 38-35.[23] Bolton led both teams with eight solo tackles and 9.0 total tackles, and he returned a fumble by Jalen Hurts 36 yards for a touchdown.[24]
During the 2023 season, Bolton recorded 60 total tackles, one interception, and three passes defended. Bolton helped the Chiefs reach Super Bowl LVIII where they defeated the San Francisco 49ers 25–22 to repeat as Super Bowl champions.[25] Bolton led both teams with 13 total tackles.[26]
During Week 13 of the 2024 season, Bolton recorded 11 tackles and recovered a fumble from Raiders quarterback Aidan O'Connell with 14 seconds left in the game. This would, in essence, end the game and send the Kansas City Chiefs to the playoffs, marking their 10th straight appearance in the postseason. [27]