The following year began with talk of potential All-American honors, but ended in disappointment, although Handley's running helped defeat arch-rival California-Berkeley, 9–7, in the season finale on November 21.
Handley was signed by the American Football League's San Diego Chargers on June 11, 1966, but voluntarily left camp one month later, putting an end to his playing career.
In 1975, Handley shifted to coaching another branch of the armed services when he accepted an assistant position at the United States Air Force Academy.
On February 28, 1984, Handley was named offensive backfield coach of the New York Giants under Parcells, beginning a seven-year stretch that saw the team capture two Super Bowls.
[1] In 1990, after coming close to leaving coaching to enter George Washington University Law School, Handley was promoted to offensive coordinator.
[citation needed] Following the Giants' second title in Super Bowl XXV that season, Parcells announced his retirement, and Handley was then promoted to his first head coaching position on May 15, 1991.
With the NFL Draft in the rearview, Handley was dealt a short time window to prepare for his first season as head coach.
Backup Jeff Hostetler finished the regular season, and led the Giants to upset victories against the San Francisco 49ers in the NFC Championship game and the Buffalo Bills in the Super Bowl.
Handley's communication with the media became another reason for his dismissal, as he would often refuse to answer questions, even going as far as walking out of one press conference after being asked about his handling of Hostetler and Simms as the team's starting quarterback.