Downing received his first coaching job, and was an assistant coach for Eden Prairie High School as a 9th grade B team offensive coach. While coaching his high school, the Eagles won the Class 5A state title in 2000 over Matt Birk's Cretin Durham Hall Raiders. After being offered an internship in 2001 by Chad Ostlund in Research and Development for the Minnesota Vikings. He was a Public Relations intern for 2002. a football systems analyst from 2003–04, and as the offensive quality control coach in 2005. In 2006, Downing was hired by the then St. Louis Rams to be a Special Teams/Defensive assistant coach. He would keep this job for two seasons. In 2008 Downing would become the Rams defensive quality control coach. Downing went to the Detroit Lions with Scott Linehan as an offensive quality control coach in 2009. He was the assistant quarterback coach in 2010 and was promoted to the quarterbacks coach role from 2011–2013. While he was coaching quarterbacks in Detroit, Matthew Stafford averaged 4,885 yards, thirty touchdowns, and seventeen interceptions from 2011–2013. Downing was the Buffalo Bills' quarterback coach in 2014, and took the same job for the Oakland Raiders in 2015. He is credited for helping Derek Carr become the first Raiders quarterback to be selected to a Pro Bowl since 2002. On January 20, 2015, Downing was named by Pro Football Focus as Quarterbacks Coach of the Year. After coaching Raiders quarterbacks for two years, he was promoted to offensive coordinator in 2017, after the Raiders decided not to renew Bill Musgrave's contract. When he coached Carr from 2015–2016, he threw for 7,924 yards, sixty touchdowns, and nineteen interceptions with two Pro Bowl appearances. Downing was fired on January 1, 2018, along with head coachJack Del Rio and the rest of Del Rio's staff after dropping from 12–4 to 6–10 due to a major regression of the offense. On February 19, 2018, Downing was hired by the Minnesota Vikings as a senior offensive assistant.. Following the sudden passing of Vikings offensive line coachTony Sparano prior to training camp in 2018, tight ends coach Clancy Barone was shifted to coach the offensive line, alongside Sparano's assistant offensive line coach, Andrew Janocko. Downing was moved from senior offensive assistant to tight ends coach to fill the vacant position. On January 26, 2019, Downing was hired by the Tennessee Titans as their tight ends coach.
Playing career
He played quarterback for the Minnesota Maulers, a semi-pro football team from 2000 to 2002. Todd played Quarterback and defensive back while helping the Maulers to 3 consecutive championship games.