Walsh left the Raiders the next year to become the head coach and general manager of the San Jose Apaches of the Continental Football League (CFL).

He led the Apaches to second place in the Pacific Division, but the team ceased all football operations prior to the start of the 1968 CFL season.

Cincinnati's new quarterback, Virgil Carter, was known for his great mobility and accuracy but lacked a strong arm necessary to throw deep passes.

To suit his strengths, Walsh suggested a modification of the downfield based "vertical passing scheme" he had learned during his time with the Raiders with one featuring a "horizontal" approach that relied on quick, short throws, often spreading the ball across the entire width of the field.

Ken Anderson eventually replaced Carter as starting quarterback, and, together with star wide receiver Isaac Curtis, produced a consistent, effective offensive attack.

His notable players at Stanford included quarterbacks Guy Benjamin, Steve Dils, wide receivers James Lofton and Ken Margerum, linebacker Gordy Ceresino, and running back Darrin Nelson.

Hidden behind that record were organizational changes made by Walsh that set the team on a better course, including selecting Notre Dame quarterback Joe Montana in the third round of the 1979 NFL draft.

The contest was very close, and in the fourth quarter Walsh called a series of running plays as the 49ers marched down the field against the Cowboys' prevent defense, which had been expecting the 49ers to mainly pass.

The 49ers came from behind to win the game on Joe Montana's pass completion to Dwight Clark for a touchdown, a play that came to be known simply as The Catch, propelling Walsh to his first appearance in a Super Bowl.

Two weeks later, on January 24, 1982, San Francisco faced the Cincinnati Bengals in Super Bowl XVI, winning 26–21 for the team's first NFL championship.

In all, Walsh served as 49ers head coach for 10 years, winning three Super Bowl championships, in the 1981, 1984, and 1988 seasons, and establishing a new NFL record.

[13] In addition to Joe Montana, Walsh drafted Ronnie Lott, Charles Haley, and Jerry Rice, each one going on to the Pro Football Hall of Fame.

He also traded a 2nd and 4th round pick in the 1987 draft for Steve Young, who took over from Montana, led the team to Super Bowl success, and was enshrined in Canton after his playing career.

On January 22, 1989, Walsh coached his final game with the 49ers, the memorable Super Bowl XXIII in which San Francisco beat Cincinnati 20–16.

Dennis Green trained Tony Dungy, who won a Super Bowl with the Indianapolis Colts, and Brian Billick with his brother-in law and linebackers coach Mike Smith.

Gruden himself would train Mike Tomlin, who led the Pittsburgh Steelers to their sixth Super Bowl championship, and Jim Harbaugh, whose 49ers would face his brother, John Harbaugh, whom Reid himself trained, and the Baltimore Ravens at Super Bowl XLVII, which marked the Ravens' second World Championship.

First, according to a February 2015 article by Mike Florio of NBC Sports, after a 5–11 season in 1989, the Patriots fired Raymond Berry and unsuccessfully attempted to lure Walsh to Foxborough to become head coach and general manager.

[18] Second, late in the 1990 season, Walsh was rumored to become Tampa Bay's next head coach and general manager after the team fired Ray Perkins and promoted Richard Williamson on an interim basis.

Part of the speculation was fueled by the fact that Walsh's contract with NBC, which ran for 1989 and 1990, would soon be up for renewal, to say nothing of the pressure Hugh Culverhouse faced to increase fan support and to fill the seats at Tampa Stadium.

However, less than a week after Super Bowl XXV, Walsh not only declined Tampa Bay's offer, but he and NBC agreed on a contract extension.

[19] Meanwhile, after unsuccessfully courting then-recently fired Eagles coach Buddy Ryan or Giants then-defensive coordinator Bill Belichick to man the sidelines for Tampa Bay in 1991, the Bucs stuck with Williamson.

On January 15, 1992, Walsh agreed to return to Stanford to serve as their head coach with a five year contract with an annual salary of $350,000 to replace Dennis Green; he immediately named Terry Shea as offensive coordinator.

Stanford finished the season with a victory over Penn State in the Blockbuster Bowl on January 1, 1993, and a #9 ranking in the final AP Poll.

He also acted as a consultant for his alma mater San Jose State University in their search for an athletic director and Head Football Coach in 2005.

[29] Super Bowl XLII was also dedicated to Walsh's memory; at the end of the player introduction ceremonies, his son, Craig, accompanied by Ronnie Lott, Jerry Rice and Steve Young, performed the ceremonial coin toss with New York Giants captain Michael Strahan, playing his final career NFL game, calling the toss on behalf of his Giants co-captains and the New England Patriots' captains.