Horton began his coaching career after graduating from Central Washington, serving as a defensive analytics assistant with the Vanderbilt Commodores in 2015.[6] He then served one year as a defensive assistant and assistant quality control coach for the Cleveland Browns in the National Football League (NFL), being under his father who was team's defensive coordinator.[3][5][7] In 2017, he served as a summer assistant with the Pittsburgh Steelers before returning to Vanderbilt as a defensive analyst.[6]
Horton was a graduate assistant with the Southeastern Louisiana Lions in 2018.[5] The following spring, he served as the secondary coach and a defensive assistant for the Atlanta Legends of the Alliance of American Football (AAF) prior to the league folding.[8] Afterwards, he was named the coach of the star, nickel and dime cornerbacks for the UConn Huskies.[9] Horton served in those positions through 2021, when he was promoted to interim defensive coordinator and safeties coach at the start of that season after Lou Spanos became interim head coach.[2]
In 2022, Horton was named the defensive coordinator for the Pittsburgh Maulers of the United States Football League (USFL).[10] In his first season with the team, they went 1–9 and placed last in their division.[11] His father, Ray, was named the Maulers' head coach for the 2023 season.[3] Jarren Horton had said that his dream growing up was to be defensive coordinator for the Pittsburgh Steelers with his father as head coach.[3] In his second year, he helped Pittsburgh have the best defense in the league, with them having the lowest total of yards allowed per game (257.4) while having the highest number of takeaways (20).[12] Three Mauler defenders were named to the All-USFL team and they made it to the playoffs for the first time in their history, and for this Horton was named the inaugural winner of the USFL Assistant Coach of the Year Award.[12] On January 1, 2024, it was announced the Maulers would not be a part of the UFL Merger.[13]