Rush then became an assistant with the New York Jets of the American Football League in 1963, serving as the main architect of the team's high-powered offense that was later led by Joe Namath. As offensive coordinator, he reached the high point of his career when he mapped the Jets' game plan as they upset the Baltimore Colts in Super Bowl III on January 12, 1969. That success resulted in his hiring by the Patriots 18 days later. Another finalist for the job was Colts secondary coach Chuck Noll, who was hired a few days later by the Pittsburgh Steelers.
His tenure with the Patriots was marked by constant conflict with players, owners, league officials and the media. One bizarre indication of Rush's luck came on February 12, 1969, when he introduced the team's new general manager, George Sauer, Sr. While grabbing the microphone, Rush received a five-second electrical shock that left him briefly stunned.
During his 21 games as Patriots' head coach, his team won only five contests. During the team's sixth straight loss of the 1970 NFL season, a 45–10 defeat to the Buffalo Bills on November 1, 1970, Rush began to suffer an irregular heartbeat and briefly left the stadium. Two days later, he resigned as head coach and said he would never coach again.
However, in March 1971, he was hired by George Allen, who had recently taken the helm of the Washington Redskins. Just six weeks later, Rush abruptly resigned and was out of football for the next five years.
Rush resurfaced as the head football coach at the United States Merchant Marine Academy in 1976. While he led the team to an 8–1 record, complaints from players resulted in his firing after only one season. Rush did not coach the final two games.