The rivalry stems from the proximity of Oakland and San Francisco in the northern Bay Area, and was formalised the first time the teams met after the AFL–NFL merger in the 1970 season.

This disparity showed when the two teams met again on October 27, 1974, where the Raiders beat the 49ers 35–24 at Candlestick Park in a showoff between Ken Stabler and Tom Owen.

Meanwhile, the 49ers struggled to finish seasons with a winning record, going through a coaching carousel of Dick Nolan, Monte Clark, Ken Meyer, and Pete McCulley.

In 1979, both teams acquired new head coaches, with Bill Walsh taking over for the 49ers and Tom Flores replacing John Madden for the Raiders.

That same year, the 49ers with Montana under center led a dramatic comeback in the NFC championship to earn their first ever Super Bowl appearance, which they won against the Cincinnati Bengals.

The Raiders were stifled in the wild card round by the Seattle Seahawks, and the 49ers won Super Bowl XIX against Dan Marino's Miami Dolphins.

The Niners began the season struggling in 1988, with Joe Montana and Steve Young competing for the starting job after a poor performance by the former in 1987.

On November 3, 2002, the 49ers defeated the Raiders 23–20 in overtime at the Oakland Coliseum with Jose Cortez kicking a 23-yard field goal to win the game.

On October 8, 2006, the 49ers beat the Raiders 34–20 at Candlestick with Oakland quarterbacks Andrew Walter and Marques Tuiasosopo throwing four interceptions, three of which were by Walt Harris.

On November 1, 2018, the 49ers, led by practice squad quarterback Nick Mullens, defeated the Raiders by a score of 34–3, ending a six-game losing streak.

Prior to the 2011 NFL season, the 49ers and Raiders regularly held a joint practice and then met during the preseason as a manifestation of their geographic rivalry.

[17] In 2024, the Raiders hosted Super Bowl LVIII in Allegiant Stadium, whose contenders were later determined to be their rivals the 49ers and the Kansas City Chiefs.