1970s

Teams of the former American Football League were merged into the National Football League in 1970, setting up the first ever matchup between the 49ers and Raiders. Heading into the season finale, the 49ers (9–3–1) needed a win over the Raiders (8–3–2) to clinch the NFC West. On December 20, 1970, the Raiders were blown out by the 49ers 38–7 at Oakland Coliseum, as John Brodie threw for three touchdowns and Jimmy Johnson picked off Daryle Lamonica for a touchdown. Regardless, both teams managed to advance to (and lose) their respective conference championships.

In the earlier half of the 1970s, both teams were consistent performers, the Raiders becoming known as a hard-hitting, fierce team while the 49ers consistently dominated the NFC West. However, although the Oakland Raiders continued to improve, consistently clinching spots in the AFC championship, the 49ers began to regress. 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. The Niners turned over the football five times.

The John Madden-led Raiders continued a streak of excellence during the latter half of the 1970s, with the Raiders winning Super Bowl XI in 1976. 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. On November 4, 1979, the Raiders beat the 49ers 23–10, with Cliff Branch hauling in two touchdowns from Ken Stabler.

1980s

Although the Walsh-led Niners suffered losing seasons in 1979 and 1980 and the Raiders won Super Bowl XV in 1980 as the first wild-card team to win the Super Bowl, their fortunes were about to change. In 1980, Raiders owner Al Davis's failure to get luxury boxes added to the Oakland-Alameda County Coliseum resulted in a hard-fought legal battle that made 1981 the Raiders' last year in Oakland. 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.

In 1982, the defending Super Bowl champion 49ers floundered, losing all of their home games, including the first game of the season against the newly minted Los Angeles Raiders, which the Raiders won on the back of Marcus Allen, who rushed for 116 yards.

Two years later, in 1984, the Niners had one of the most phenomenal seasons in NFL history, finishing the regular season 15–1–0, a feat that has only been repeated or exceeded five times. 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 Raiders and Niners met again on September 22, 1985, with San Francisco's defense obliterating the Raider offense, with Jim Plunkett tasting turf nine times, resulting in a 34–10 blowout of the Raiders at the Los Angeles Coliseum.

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. In their match against the Raiders on November 13, 1988, they were defeated 9–3, with Montana sacked four times (with the help of Reggie McKenzie, who is the Raiders' general manager as of 2017). The 49ers turned their season around and won Super Bowl XXIII against the Cincinnati Bengals 20–16. San Francisco repeated their Super Bowl championship the next season, trampling the Denver Broncos 55–10.

In the meantime, Al Davis began negotiations to return the Raiders to Oakland.

1990s

In March 1991, Davis announced that he was moving the Raiders back to Oakland, but Los Angeles reached a deal with him to keep the Raiders at the Coliseum later in the year. On September 29, 1991, the 49ers met the Raiders again in Los Angeles, with the Raiders winning 12–6 against a touchdown-less Steve Young San Francisco offense.

The season opener of 1994 at Candlestick Park was the next iteration in the rivalry, with the 49ers beating the Raiders 44–14. In 1994's Super Bowl XXIX, the 49ers won their last Super Bowl to date against the then-San Diego Chargers. The next year, the Los Angeles Raiders returned to Oakland.

2000s

On October 8, 2000, Oakland defeated San Francisco 34–28 in overtime with Rich Gannon connecting with Tim Brown for 2 touchdowns and the Niners' Jeff Garcia passing for four touchdowns. 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.

2010s

On October 17, 2010, the 49ers defeated the Raiders 17–9, giving them their first win of the season after a 5-game losing streak. Raiders quarterback Jason Campbell was held to just 83 yards passing. In 2012, the 49ers under Colin Kaepernick lost Super Bowl XLVII to the Baltimore Ravens, with Kaepernick becoming permanent starter after Alex Smith suffered a concussion in Week 10.

On December 7, 2014, the Derek Carr-led Raiders broke their three-game losing streak against the 49ers with a 24–13 win at the Oakland-Alameda County Coliseum.

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. Mullens, who had his NFL debut, previously played and provided a game-winning touchdown in a preseason game against the Dallas Cowboys. This game concluded the "Battle of the Bay," the nickname for the geographical rivalry.

On January 1, 2023, the 49ers won the game 37–34 in overtime after the Raiders threw an interception. The loss eliminated the Raiders from the playoffs.^[14]