Johnson, 81, had been in declining health, according to family members.
After one year in the Canadian Football League, Johnson entered the NFL in 1954 as a member of the 49ers' vaunted "Million Dollar Backfield," which also included running backs Joe "The Jet" Perry (who passed away in April at 84) and Hugh McElhenny and quarterback Y.A. Tittle. The group remains the only full-house backfield to have all four of its members enshrined in the Pro Football Hall of Fame.
"I was deeply saddened to hear of John Henry Johnson's passing," 49ers owner John York said Saturday in a statement released by the team. "He was a good friend, not only to my family and me, but the entire 49ers organization. As a member of 'The Million Dollar Backfield,' he holds a cherished place in both 49ers and NFL history. His contributions to the game of football will be forever celebrated. Our heartfelt sympathy goes out to the entire Johnson family."
In 1957, the 49ers traded Johnson to the Lions, who won the NFL championship that year. He was dealt to the Steelers, who originally drafted him, in 1960, then had his finest statistical seasons, running for 1,141 yards in 1962 and 1,048 yards in 1964. He was the first Steeler to break the 1,000-yard barrier.
"We are deeply saddened by the death of John Henry Johnson," the Steelers said Saturday in a statement, via the Pittsburgh Post-Gazette. "He was one of the Steelers' great running backs, evident by being the team's first 1,000-yard rusher in 1962. ... John Henry was one of the first in a long line of Steelers' Hall of Famers. The entire Steelers organization sends its condolences to the Johnson family for the loss of one of the great players in team history."
Johnson spent the 1966 season with the AFL's Oilers before retiring. At that time, he trailed only Jim Brown, Jim Taylor and Perry on the NFL's career rushing yards list. Johnson now ranks 55th.
Johnson also made 186 receptions for 1,478 yards, and he scored 55 touchdowns. He made the Pro Bowl four times, in 1955, 1963, 1964 and 1965.
Johnson wasn't just a good runner and pass catcher. He also was a feared blocker, leading Hall of Fame quarterback Bobby Layne, who played with Johnson in Detroit and Pittsburgh, to say: "John Henry is my bodyguard. Half the good runners will get a passer killed if you keep them around long enough. But a quarterback hits the jackpot when he gets a combination runner-blocker like Johnson."
"I speak on behalf of all of John Henry's fellow Hall of Famers, our board and staff, in sending our condolences to the Johnson family," Steve Perry, the Hall of Fame's president and executive director said in a statement. "John Henry's place in football history as one of the game's most punishing runners and greatest blockers will forever be remembered through his bronze bust in the Hall of Fame."
The Associated Press contributed to this report.