Even with fill-ins, 49ers’ run defense remains solid

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When Cowboys running back DeMarco Murray gashed the 49ers’ shorthanded defense for 118 yards in Week 1, it appeared to be a bad omen.

Nope. Try an aberration.

Since its uneven season-opening performance, the 49ers’ run defense has been impenetrable: It has allowed a total of 152 rushing yards in the past three games, the fewest the 49ers have allowed in a three-game span since 1997.

Outside linebacker Dan Skuta, who was 11 in 1997, smiled when he heard that statistic Tuesday.

“I think some stats you don’t pay attention to and some you like because run defense kind of shows you the mind-set of your defense,” Skuta said. “So if you’re playing the run well, you know you’re playing tough and you’re playing physical.”

The 49ers’ run defense has specialized in tough and physical for several seasons. From 2011 to 2013, the 49ers allowed the fewest yards per game (89.1) and yards per carry (3.7). Last season, they were the only team to not allow a 100-yard rusher during the regular season.

But that was with All-Pro linebackers NaVorro Bowman (now recovering from a knee injury) and Aldon Smith (now suspended), who will miss a minimum of 15 games combined this season. In addition, nose tackle Glenn Dorsey (biceps injury), who started 13 games last year, will miss at least eight games.

The 49ers’ pass rush has certainly been diminished without Smith, but it’s hard to detail any drop-off in their vaunted run defense.

Eagles running back LeSean McCoy was stopped for a loss by Demarcus Dobbs (83). The San Francisco 49ers defeated the Philadelphia Eagles 26-21 at Levi's Stadium Sunday September 28, 2014. Eagles running back LeSean McCoy was stopped for a loss by Demarcus Dobbs (83). The San Francisco 49ers defeated the Philadelphia Eagles 26-21 at Levi's Stadium Sunday September 28, 2014. Photo: Brant Ward / The Chronicle Photo: Brant Ward / The Chronicle Image 1 of / 1 Caption Close Even with fill-ins, 49ers’ run defense remains solid 1 / 1 Back to Gallery

They have allowed 2.7 yards per carry in their past three games, and their competition (Bears, Cardinals and Eagles) makes that figure even more impressive: Philadelphia’s LeSean McCoy and Chicago’s Matt Forte ranked first and second, respectively, in rushing yards in 2013, and Arizona’s Andre Ellington had the most yards per carry (5.5) among running backs with at least 100 attempts.

This wasn’t supposed to happen with two undrafted free agents from Division II colleges subbing for stars: Skuta, 28, has assumed Smith’s spot in the base defense, and Michael Wilhoite, 27, is filling in for Bowman.

Wilhoite said he has settled into a rhythm with fellow inside linebacker Patrick Willis, a seven-time Pro Bowl selection.

“It’s having confidence in myself and (Willis) having confidence in me that I can do the job on my side,” Wilhoite said. “He can trust that I’m going to be where I need to be so he doesn’t have to do anything extra. He can just do his job, and I’ll do my job, and we can count on each other. I think a lot of that just comes with experience and with snaps. And we’re comfortable right now.”

Sunday, McCoy averaged 1.7 yards per carry and the Eagles had 22 rushing yards, the ninth-fewest the 49ers have allowed in their franchise history. Last year, when Wilhoite was subbing for the injured Willis during a two-game stretch, the 49ers allowed the seventh-fewest rushing yards (18) in franchise history in a win at St. Louis.

In other words, the 49ers’ run defense has been historically dominant in two of Wilhoite’s six career starts. Wilhoite, who ranks third on the team in tackles (15), will lose his starting spot when Bowman returns. In the meantime, Bowman is serving as his unofficial coach while forecasting a starting role in his future.

“I let him know that. This is his chance to put tape out there and show people that he can play in the NFL,” Bowman said. “I’m excited for him.”

For his part, Wilhoite is excited for the next challenge. On Sunday, the 49ers will host the Chiefs and Jamaal Charles. Kansas City’s running back ranked third in the NFL in rushing in 2013 and is coming off a 92-yard, three-touchdown performance in a 41-14 win over New England on Monday.

“It’s not about showing that I can play like Bow or Pat — that I’m as good as them or better,” Wilhoite said. “It’s just going out there and playing good football so we can go out there and win games. That’s it. That’s where my pride is — in winning games.”

Eric Branch is a San Francisco Chronicle staff writer. E-mail: ebranch@sfchronicle.com

Run stoppers, now and then

The 49ers have allowed 152 rushing yards in their past three games, the fewest they’ve allowed in a three-game span since 1997. A look at the two streaks:

2014

9/14 vs. Chicago: 17 atts., 46 yds.

9/21 at Arizona: 27 atts., 84 yds.

9/28 vs. Philadelphia: 12 atts., 22 yds.

Totals: 56 atts., 152 yds., 2.7 yds. per carry

1997

10/12 vs. St. Louis: 13 atts., 30 yds.

10/19 at Atlanta: 16 atts., 39 yds.

10/26 at New Orleans: 18 atts., 55 yds.

Totals: 47 atts., 124 yds., 2.6 yds. per carry