The 49ers announced Tuesday that McVay had died. They did not give a cause of death.
McVay spent 22 seasons with the 49ers starting in 1979 in various capacities. He played an integral role along with coach Bill Walsh in building one of the league's greatest dynasties that won five Super Bowl titles in a span of 14 seasons.
"This is a very sad day for our organization and the entire football community," the team said in a statement. "John McVay was a driving force in constructing teams for our five Super Bowl titles. Most importantly, John was a Hall of Fame person who built genuine and sincere relationships with front office staff, coaches and players. John's commitment and contributions to the 49ers created the standard and tradition we strive to carry on today. Our thoughts and prayers are with the McVay family."
McVay was inducted into the 49ers Hall of Fame in 2013, and the team dedicated its draft room as the "John McVay Draft Room" in his honor in 2016.
McVay originally joined the Niners in 1979 with Walsh as the director of player personnel. Over the next 17 seasons he had various titles including general manager and director of football operations. He played a role in building the NFL's model organization with players like Joe Montana, Ronnie Lott, Jerry Rice and Steve Young.
McVay was named The Sporting News NFL Executive of the Year in 1989 following the team's fourth Super Bowl title. After retiring following the 1995 season, he later rejoined the organization officially in 1999 and served as vice president and director of football operations through the 2003 season.
Before joining the 49ers, McVay was the coach of the Giants for two-plus seasons. He had a 14-23 record for New York and his most memorable game featured a late fumble by Joe Pisarcik when the Giants could have kneeled out the clock. Herm Edwards returned it for a winning TD for Philadelphia in a 19-17 win on Nov. 19, 1978, that is now known as the "Miracle at the Meadowlands."
"John was an outstanding executive and a class act," Giants co-owner John Mara said in a statement. "He was a Hall of Famer professionally and especially as a person."
McVay's grandson, Sean, followed him into the NFL and became head coach of the Niners' NFC West rival, the Rams, in 2017. Sean McVay has been to two Super Bowls and won his first title and the sixth for the family last season.
"John was such an instrumental influence on Sean and his leadership qualities permeate our entire organization through the relationship he had with his grandson,'' the Rams said in a statement. "John's legacy will live on forever and the marks he left on his family, our league, and our game will never be forgotten.''
The Associated Press contributed to this report.