Horton accepted a football scholarship from the University of Washington, where he played as a cornerback and special teams from 1980 to 1982 after a redshirt year. As a sophomore, he started 9 games. As a junior, he was a first-team All-Pac 10 selection and honorable-mention All-American. In his last year he started 9 games, missing 3 contests with an ankle injury. He finished as a three-year starter with 10 career interceptions, 22 passes defensed, including 14 in 1981 and played in two Rose Bowls. He was also one of the top punt returners in the nation.
Professional career
Cincinnati Bengals
Horton was selected by the Cincinnati Bengals in the second round of the 1983 NFL Draft. He also was selected by the Los Angeles Express in the third round of the 1983 USFL Draft. He earned the job as a starting cornerback by the second game of the season and finished with a franchise rookie record of 5 interceptions, including one returned for a touchdown. The next year, he was named the regular starter at right cornerback after the retirement of Ken Riley, posting 66 tackles and 3 interceptions, including one returned for a touchdown. In 1986, he was passed on the depth chart by rookie Lewis Billups and was moved to the nickel back role, making 55 tackles and one interception. The next year he started 8 games, while replacing an injured Louis Breeden, tallying 53 tackles. In 1988, he was moved to safety and played mainly nickel back. He recorded 26 tackles, 3 interceptions and one sack. In Super Bowl XXIII, after being up 13–6 over the San Francisco 49ersat the beginning of the fourth quarter, driving from the Bengals 10-yard line, quarterback Joe Montana threw a pass towards Billups that he dropped in the end zone. On the next play, the 49ers scored a touchdown, tying the game at 13. Towards the game's conclusion, Montana threw a 10-yard touchdown pass to John Taylor who was being covered by Horton, for a 20–16 lead with 34 seconds left and the eventual championship. He also was the team's punt returner during the game.
On March 14, 1989, the Dallas Cowboys signed Horton as a Plan B free agent with the intention of playing him at safety. He was named the starting free safety, helping anchor the secondary and calling the defensive signals. He collected 116 tackles, 8 passes defensed, 2 forced fumbles, one interception and one sack. In 1990, he sprained his left knee in the fourth game against the New York Giants, that forced him to miss one contest and slowed him the rest of the season. He posted 69 tackles, 6 passes defensed, one interception and 4 fumble recoveries. In 1991, he finished third on the team in tackles, recorded 8 passes defensed, one interception and scored in back-to-back games: a fumble return in a 21-16 win against the New York Giants and a 65-yard interception return in a 20-17 win over the Green Bay Packers. He became the first player in franchise history to score a defensive touchdown in back-to-back games and the third player ever to have 2 defensive touchdowns in the same season. In 1992, he started the first 7 games before tearing his right ACL and missing 4 games. He was replaced with James Washington who took over the starting job. He still was able to be part of the championship team in Super Bowl XXVII. Horton was released on June 1, 1993, with the Cowboys looking to give more opportunities to Washington and Darren Woodson. He finished his career with 19 interceptions, 11 fumble recoveries, 3 sacks and 5 defensive touchdowns.
Coaching career
Horton began his coaching career in 1994 as a defensive assistant with the Washington Redskins. He was hired by Norv Turner, who knew him from Dallas where Turner was an Offensive Coordinator. Horton was the defensive backs coach for the Bengals and Detroit Lions. He was the assistant defensive backs coach for the Pittsburgh Steelers from 2004-2006 before being promoted to defensive backs coach in 2007. On February 9, 2011, Horton was named defensive coordinator for the Arizona Cardinals. In 2013, Arizona head coach Ken Whisenhunt was fired, though Horton was initially retained and considered for promotion to head coach. On January 17, 2013, Horton was passed over for the promotion in favor of his former fellow assistant at Pittsburgh Bruce Arians, leading to his prompt departure from Arizona. On January 18, 2013, Horton was hired as the defensive coordinator of the Cleveland Browns. On January 18, 2014, Horton agreed to become the defensive coordinator of the Tennessee Titans. Browns coach Hue Jackson hired Ray Horton to be the Browns defensive coordinator going into the 2016 season. After a single season, Horton was fired by the Browns on January 7, 2017. He was hired as the Redskins' defensive backs coach on January 24, 2019.
