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. On May 13, 2021, Bolton officially signed with the Chiefs on a $5.84 million deal. Bolton was put on the Reserve/
COVID-19 list on December 21. He was activated on December 25. In Week 18, against the
Denver Broncos, he recorded his first NFL touchdown on an 86-yard fumble return in the 28–24 victory. As a rookie, he appeared in 16 games and started 12. He finished with 112 total tackles and three passes defended. He was named to the 2021 PFWA All-Rookie Team. During the 2022 season, Bolton recorded two sacks, 180 total tackles (108 solo), two interceptions, three passes defended, and one forced fumble. He finished second in the NFL in combined and solo tackles in the 2022 season, helping the Chiefs reach
Super Bowl LVII. Bolton then played a key role in their 38–35 victory over the
Philadelphia Eagles, leading both teams with nine total tackles, and returning a fumble by
Jalen Hurts 36 yards for a touchdown. During the 2023 season, Bolton recorded 60 total tackles, one interception, and three passes defended. The Chiefs reached
Super Bowl LVIII where they defeated the
San Francisco 49ers, 25–22, to repeat as
Super Bowl champions. Bolton led both teams with 13 total tackles. During Week 13 of the 2024 season against the
Las Vegas Raiders, 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 Chiefs to the playoffs, marking their 10th straight appearance in the postseason. He finished the 2024 season with three sacks, 106 total tackles (73 solo), one interception, six passes defended, one forced fumble, and two fumble recoveries. However, in
Super Bowl LIX, a rematch of Super Bowl LVII, the Chiefs lost to the Eagles, 40–22, erasing their hopes of becoming the first NFL team to win three consecutive Super Bowls. Bolton recorded nine tackles in the game, as he did the first time he took on the Eagles in the Super Bowl. On March 14, 2025, Bolton re-signed with the Chiefs on a three-year, $45 million contract. He finished the 2025 season with one sack, 154 total tackles (73 solo), one interception, and six passes defended. ==Career statistics==