Widenhofer returned to the NFL for six years as an assistant coach, serving as defensive coordinator for the Detroit Lions under head coach Wayne Fontes, followed by two years as linebackers coach with the Cleveland Browns under head coach Bill Belichick. He then joined friend Rod Dowhower's staff at Vanderbilt to serve as defensive coordinator. When Dowhower was fired after the 1996 season, Widenhofer was promoted to head coach. In 1997, his Vanderbilt team led the SEC in total defense. However, his second tenure as head coach was no easier than the first, as Widenhofer compiled only a 15–37 record in five seasons at the helm for VU. Widenhofer resigned in 2001. While unsuccessful on the field, the NCAA announced that Vanderbilt led the nation in football graduation percentage with a perfect 100% the year he left.