49ers give up 312 rushing yards to Bills, just 12 yards shy of franchise record

If you play fantasy football, it is a good strategy to start any running back that is facing the San Francisco 49ers' defense this season. Like every game over their past five losses, the San Francisco run defense had another bad day. They have allowed a 100-yard rusher in each game during their five-game losing streak. As if that was not enough to put some job security doubt into defensive coordinator Jim O'Neil's mind, the 49ers defense outdid themselves during their 45-16 blowout loss to the Buffalo Bills on Sunday.

O'Neil's unit allowed 312 yards rushing to the Bills. According to Matt Maiocco of CSN Bay Area, that total was just 12 yards shy of the worst mark in franchise history. What record did it approach? The 49ers gave up 324 rushing yards to the Los Angeles Rams ... in 1958. That's right. They 49ers defense nearly broke a team record that was 58 years old.

The 49ers defense has allowed 1,046 rushing yards to opponents through six games. They are on pace to allow 2,789 this season. How bad is that? It's 769 yards more than Eric Mangini's defense from a season ago allowed. San Francisco has the worst run defense in the league after using back-to-back first-round picks on defensive lineman.

RELATED Recap: 49ers have no answer for LeSean McCoy, Bills in 45-16 loss

Bills running back LeSean McCoy accounted for 140 of those yards to go along with his three touchdown runs against his former head coach. Backups Tyrod Taylor and Mike Gillislee accounted for another 128. The Bills averaged 7.1 yards per rushing attempt and were tackled for a loss just four times.

Many fans have been clamoring for Marcus Rush, the preseason standout who is currently on the practice squad, to get activated and see some playing time because of his pass rushing skills. However, the one knock on Rush was his inability to defend the run. The 49ers run defense is already bad enough. While help with the pass rush would be welcome, it's the run defense that is hurting the team the most.

"It is embarrassing to have the ball run on you like that when you know they're going to run the ball," said S Eric Reid following the loss.

"I think we've got to do a better job as coaches to put our guys in position to make plays," head coach Chip Kelly said regarding the 49ers' poor run defense this season.

Given his track record, the hiring of O'Neil seemed like an odd move given his track record. A dominant Week 1 performance against the Los Angeles Rams at home paused all of the criticism. Since then, O'Neil's critics have become more vocal and one has to wonder how long he has left as the team's defensive coordinator.

Kap's Return

49ers quarterback Colin Kaepernick returned to the starting lineup for the first time since November 1, 2015.

"I thought he was ok," Kelly said of Kaepernick. "There are some positives that you can really build with him that I thought he did. I thought he extended some drives keeping plays alive with his legs."

It was a tale of two halves for the quarterback. Kaepernick started the game well, completing 8 of 11 passes for 135 yards and a touchdown. During the second half, he was just 5 of 18 for 52 yards as the Bills outscored the 49ers 28 to 3 following the intermission.

"It was an ugly season debut for Kaepernick, who in addition to being inaccurate for much of the day also made a few careless plays," said Steve Slowik of Pro Football Focus. "Kaepernick's 59.3 adjusted completion percentage was the worst among all QBs through the 1:00 pm Sunday games and he really struggled to throw the ball when Buffalo was able to apply pressure, completing just four of 11 passes for 43 yards to go with a 48.7 QB rating while under duress."