Walsh died at his Woodside home Monday morning following a long battle with leukemia.
"This is just a tremendous loss for all of us, especially to the Bay Area because of what he meant to the 49ers," said Hall of Fame quarterback Joe Montana, the player most closely linked to Walsh's tenure with the team. "For me personally, outside of my dad he was probably the most influential person in my life. I am going to miss him."
Walsh didn't become an NFL head coach until 47, and he spent just 10 seasons on the San Francisco sideline. But he left an indelible mark on the United States' most popular sport, building the once-woebegone 49ers into the most successful team of the 1980s with his innovative offensive strategies and teaching techniques.
The soft-spoken native Californian also produced a legion of coaching disciples that's still growing today. Many of his former assistants went on to lead their own teams, handing down Walsh's methods and schemes to dozens more coaches in a tree with innumerable branches.
"The essence of Bill Walsh was that he was an extraordinary teacher," NFL commissioner Roger Goodell said in a statement. "If you gave him a blackboard and a piece of chalk, he would become a whirlwind of wisdom. He taught all of us not only about football but also about life and how it takes teamwork for any of us to succeed as individuals."
Walsh went 102-63-1 with the 49ers, winning 10 of his 14 postseason games along with six division titles. He was named the NFL's coach of the year in 1981 and 1984.
Few men did more to shape the look of football into the 21st century. His cerebral nature and often-brilliant stratagems earned him the nickname "The Genius" well before his election to the Pro Football Hall of Fame in 1993.
Even a short list of Walsh's adherents is stunning. Seifert, Mike Holmgren, Dennis Green, Sam Wyche, Ray Rhodes and Bruce Coslet all became NFL head coaches after serving on Walsh's San Francisco staffs, and Tony Dungy played for him. Most of his former assistants passed on Walsh's structures and strategies to a new generation of coaches, including Mike Shanahan, Jon Gruden, Brian Billick, Andy Reid, Pete Carroll, Gary Kubiak, Steve Mariucci and Jeff Fisher.
Walsh created the Minority Coaching Fellowship program in 1987, helping minority coaches to get a foothold in a previously lily-white profession. Marvin Lewis and Tyrone Willingham are among the coaches who went through the program, later adopted as a league-wide initiative.
Walsh was diagnosed with leukemia in 2004 and underwent months of treatment and blood transfusions. He publicly disclosed his illness in November 2006.
Fellow Hall of Fame coach Marv Levy, who hired Walsh to his first college coaching job, last spoke to him about six weeks ago on the telephone.
"I asked him how he was doing, and he said he had come off a certain type of a treatment and he felt much more energy," Levy said. "But he told me then, he said, 'Marv, I don't have long.' He said it honestly. He was vibrant. Understood it. And yet, I was sad to hear it."
Born William Ernest Walsh on Nov. 30, 1931 in Los Angeles, he was a self-described "average" end and a sometime boxer at San Jose State in 1952-53.
Walsh, whose family moved to the Bay Area when he was a teenager, married his college sweetheart, Geri Nardini, in 1954 and started his coaching career at Washington High School in Fremont, leading the football and swim teams.
Walsh was coaching in Fremont when he interviewed for an assistant coaching position with Levy, who had just been hired as the head coach at California.
"I was very impressed, individually, by his knowledge, by his intelligence, by his personality and hired him," Levy said.
After Cal, he did a stint at Stanford before beginning his pro coaching career as an assistant with the AFL's Oakland Raiders in 1966, forging a friendship with Al Davis that endured through decades of rivalry. Walsh joined the Cincinnati Bengals in 1968 to work for legendary coach Paul Brown, who gradually gave complete control of the Bengals' offense to his assistant.
Walsh built a scheme based on the teachings of Davis, Brown and Sid Gillman - and Walsh's own innovations, which included everything from short dropbacks and novel receiving routes to constant repetition of every play in practice.
Though it originated in Cincinnati, it became known many years later as the West Coast offense - a name Walsh never liked or repeated, but which eventually grew to encompass his offensive philosophy and the many tweaks added by Holmgren, Shanahan and other coaches.
Much of the NFL eventually ran a version of the West Coast in the 1990s, with its fundamental belief that the passing game can set up an effective running attack, rather than the opposite conventional wisdom.
Walsh also is widely credited with inventing or popularizing many of the modern basics of coaching, from the laminated sheets of plays held by coaches on almost every sideline, to the practice of scripting the first 15 offensive plays of a game.
Walsh turned over the starting job to Montana in 1980, when the 49ers improved to 6-10 - and improbably, San Francisco won its first championship in 1981, just two years after winning two games.
Championships followed in the postseasons of 1984 and 1988 as Walsh built a consistent winner and became an icon with his inventive offense and thinking-man's approach to the game. He also showed considerable acumen in personnel, adding Ronnie Lott, Charles Haley, Roger Craig and Rice to his rosters after he was named the 49ers' general manager in 1982 and the president in 1985.
He spent three years as a broadcaster with NBC before returning to Stanford for three seasons. He then took charge of the 49ers' front office in 1999, helping to rebuild the roster over three seasons. But Walsh gradually cut ties with the 49ers after his hand-picked successor as GM, Terry Donahue, took over in 2001.
He is survived by his wife, Geri, and two children, Craig and Elizabeth.
Walsh's son, Steve, an ABC News reporter, died of leukemia at age 46 in 2002.