This year's camp, the first under coach Kyle Shanahan and general manager John Lynch, has no such battle. Veteran Brian Hoyer is the unquestioned starter and has backed it up with consistently sharp performances through the first week-plus of practice.
That doesn't mean there isn't a battle brewing at quarterback at all, however. Quietly, rookie quarterback C.J. Beathard has elbowed his way into a competition with veteran Matt Barkley for the No. 2 job behind Hoyer.
“They’ve been competing," Shanahan said. "I think they’ve had even reps. I think it’s a good battle for us. We’ve been looking at it every day and they’re going to make it tough on us.”
When the Niners signed Barkley in the opening days of free agency, the expectation was he would handle the primary backup duties behind Hoyer. Even after the Niners used a third-round pick on Beathard, that seemed the most likely course of action as Beathard adjusted to the NFL.
But even as far back as the offseason program, Shanahan found himself impressed with Beathard's maturity and his ability to improve from practice to practice.
“We evaluated both through OTAs, wanted to see if he’d be ready to run with the twos a little bit more in training camp and he earned that through our 10 OTA practices and the minicamps he earned that," Shanahan said. "After we finish it all we go back and watch the tape and try to reevaluate it. We knew coming into training camp that it was what he had done at OTAs he earned the right to compete for that two spot.”
After some rough moments early in camp, Beathard has settled in recently and made the most of his opportunities to work with the second-team offense.
In each practice, the Niners have at least a couple of periods of what Shanahan calls "move the ball" drills. Those drills are the closest thing the Niners get to game action where they are running actual drives without just working from a script. It's more free flowing and puts the pressure on the quarterbacks to be on point with play calling.
For those periods, Shanahan prefers to match the No. 2 offense against the No. 1 defense and vice-versa. For Beathard and Barkley, it's a prime opportunity to build a case for the backup job.
While neither has necessarily separated from the other in those drills, both have had success in recent days. Last week, Beathard led a scoring drive that saw him making quick, easy decisions and maneuvering in the pocket on a third-down completion to keep the drive alive. He also fired a strike into coverage to tight end Cole Hikutini for a gain of about 30 yards for what was probably his best throw of camp. On Saturday, Barkley led an impressive scoring drive in which he and wideout Aldrick Robinson hooked up four times, including a well-placed throw for a touchdown that covered about 20 yards.
"In my mind, there is always a competition regardless of what your standing is on the roster," Barkley said. "I’m competing against myself, competing against C.J., Nick, Brian, the whole room. We’re all trying to make each other better. I’m just trying to outplay every one every day."
There's still a long way to go between now and the start of the regular season and while it seems unlikely the Niners would feel the need to rush Beathard into a situation where he'd be a snap away from having to play, it's not out of the question that he could earn it. With four preseason games and some joint practices against the Denver Broncos coming up, Beathard will get a chance to work against some talented defenses and see where he stands.
So far, though, nothing has seemed too big for Beathard and his experience playing in a pro-style offense at Iowa has helped speed up his transition to the NFL.
"He’s one of the few quarterbacks who actually called plays from a huddle last year," Hoyer said. "So, he’s used to having to call a play. Now, there were arm signals from the sideline or whatever. But, that’s one thing that I think, you can see C.J. is used to getting a play call, calling it in the huddle. As opposed to a guy who looks over to the sideline, never has to say anything to the offense and then goes and runs the play. I think if you were to come from a system like that and do this, you’d be swimming no matter what you did. To have to hear a play, repeat it, break the huddle and then remember all that. I could see it being tough.”