While the head coach of Boston College, Henning discovered a major sports betting scandal among his own players, the second major gambling scandal to affect Boston College athletics in less than 20 years. It had been an open secret that football players were gambling, even though NCAA rules bar any form of gambling by student-athletes. However, after a 45-17 thumping at the hands of Syracuse on October 26, 1996, Henning heard rumors that players were betting against their own team. At a team meeting later that week, Henning asked anyone who was involved in gambling to stand up. No one did so. After the Eagles lost a close game to Pittsburgh a week later—one in which they were 11-point favorites—an irate Henning demanded that anyone involved in gambling come forward. At a players-only meeting two days later, anywhere from 25 to 30 players admitted gambling, but the five that the captains suspected of betting against their own team failed to own up. Henning notified university officials of his suspicions, and they were concerned enough to call in Middlesex County district attorney Thomas Reilly, who launched an investigation.
The resulting inquiry resulted in the suspension of 13 players for the final three games of the season, and eight of them never played another down for the Eagles again. With the effects of the scandal and a 16–19–1 record after three seasons, Henning retired at the end of the 1996 season.
Henning had two stints as the offensive coordinator with the Washington Redskins (1981–82, 1987–88). He won two Super Bowl rings during this time.
Most recently, Henning was named offensive coordinator for the Miami Dolphins, throwing wrinkles in the offense which put Ronnie Brown as quarterback leading to a 38–13 win at the New England Patriots. His implementation of the "Wildcat" or single-wing offense was covered heavily by the media, and soon adopted by several other NFL teams in 2008 and 2009.
He was previously the offensive coordinator for the Carolina Panthers from 2002 until January 2007. Henning helped lead his team to the Super Bowl after the 2003 season. After the 2005 season in which the Panthers returned to the NFC Championship game, they were considered Super Bowl contenders in 2006. However, the offense struggled due to injuries and what critics deemed conservative play-calling by Henning, resulting in an 8–8 season and his firing.
His son, Dan, played college football as a quarterback at Maryland under head coach Bobby Ross. Ross also replaced the elder Henning as head coach of the San Diego Chargers following the 1991 season.