2023 Richardson was drafted in the first round by the
Indianapolis Colts with the fourth overall pick in the
2023 NFL draft. He joined
Cam Newton and
Daunte Culpepper as the only quarterbacks to have achieved a perfect RAS score (Relative Athletic Score). During his first training camp with the Colts, Richardson underwent nasal septum surgery to improve his breathing. On August 15, 2023, Richardson was named by head coach
Shane Steichen as the Colts' starting quarterback over
Gardner Minshew and
Sam Ehlinger. Richardson made his NFL debut in the season-opener against the
Jacksonville Jaguars. He threw his first touchdown pass to
Michael Pittman Jr., ran for a touchdown, and threw his first career interception to
Tyson Campbell in the 31–21 loss. During Week 2 against the
Houston Texans, Richardson ran for two touchdowns before leaving the eventual 31–20 road victory with a concussion in the second quarter as a result of a hit taken as he scored his second touchdown. On September 22, Richardson was declared out in Week 3 due to a concussion he suffered against the Texans. He returned the following week against the
Los Angeles Rams and recorded two passing touchdowns and a rushing touchdown, erasing a 23-point deficit in a 29–23 overtime loss. His rushing touchdown in this game marked the first time in NFL history that a rookie quarterback had scored a rushing touchdown in each of his first three starts. On October 9, Richardson was placed on injured reserve due to a grade three
AC joint sprain he suffered in Week 5 against the
Tennessee Titans, which was initially announced for him to miss one-to-two months. On October 18, the Colts announced that Richardson would miss the rest of the season, and he successfully underwent shoulder surgery to repair the sprain six days later.
2024 Richardson opened the season as the Colts' starter after recovering from shoulder surgery the previous year. He missed Weeks 5 and 6 with an oblique injury. In Week 8 against the Texans, Richardson completed 10 of 32 passes for 175 yards, a touchdown, and an interception. He also voluntarily took himself out for one play in the third quarter, stating that he "needed a breather" as the Colts lost 23–20. Richardson was benched the following week in favor of backup quarterback
Joe Flacco. Prior to the benching, Richardson had generated an NFL-worst 44.4% completion percentage in six games. After two losses with Flacco, the Colts announced that Richardson would be the starter for the remainder of the season, beginning in their Week 11 matchup against the
New York Jets. In his return as starter, Richardson completed 67% of his passes for a career-high 272 yards, a touchdown, and added two rushing scores, including the game-winner in the final minute as the Colts won 28–27. In Week 13, Richardson orchestrated a 19-play, 80-yard touchdown drive, capped off with a go-ahead two-point conversion with under 15 seconds left as the Colts came back to win 25–24 over the
New England Patriots. Richardson missed the final two games of the season with a back injury as the Colts missed the playoffs with a loss in Week 17 to the
New York Giants. He finished the season completing 47.7 percent of his 264 passing attempts for 1,814 yards, eight touchdowns, and 12 interceptions. He also rushed 86 times for 499 yards with six touchdowns.
2025 With the signing of quarterback
Daniel Jones in March 2025, Richardson opened the offseason in a competition with Jones for the starting quarterback job. On August 19, Jones was named the starter, with Richardson named a backup to begin his third NFL season. On October 13, Richardson was placed on
injured reserve after he fractured the
orbital bone in his eye during pregame warmups the previous day.
2026 On April 30, 2026, the Colts declined the fifth-year option on Richardson's contract, making him a free agent after the 2026 season. ==Career statistics==