SANTA CLARA — Bruce Miller constantly hears what his job entails in the NFL’s top-ranked rushing attack.

He hears it even as plays unfold, with directions coming from the guy running behind him: 49ers all-time leading rusher Frank Gore.

“I can feel him grabbing on the back of my jersey sometimes, like he’s almost steering me through there,” Miller said of his lead-blocker role.

Now 2½ seasons into his 49ers tenure, Miller has developed into not just a reliable fullback but a versatile one — and a converted defensive end from his college days at Central Florida.

“He’s made a smooth transition,” center Jonathan Goodwin said. “Hey, maybe he was a terrible defensive lineman but a good fullback back then and didn’t know it. He doesn’t get a lot of credit, but he’s huge for our offense.”

The 49ers (6-2) lead the league by rushing for 153 yards per game. When they host the Carolina Panthers (5-3) on Sunday, they’ll encounter a defense that’s expected to deploy a standard seven-man front, unlike other opponents that have flooded the line of scrimmage with extra defenders.

Figuring out which guy to block has been a learning process for Miller.

“That was the biggest thing: reading the front at the line of scrimmage when the ball is snapped and everybody’s moving,” Miller said. “How to get through there to the second level to block my guy, it was tough to learn if you’ve never done it before.”

Helping mentor him has been position coach Tom Rathman, one of the 49ers’ all-time best fullbacks, as well as Gore, who ranks seventh in the league with 618 rushing yards this season.

“I tell him to read it like he’s running the ball,” Gore said. “It’s common sense: read and react.”

Miller hasn’t been a true running back since his freshman year in high school, however. Even then, he said, he saw action only in practice.

But last game, Miller got his chance to run with the ball into a wide-open field.

On the second snap of their 42-10 win over the Jacksonville Jaguars in London, the 49ers called “Big Sleeper,” a play in which Miller dupes the defense by pretending he’s running to the bench before the snap.

Miller stopped short of the sideline and was uncovered long enough for Colin Kaepernick to throw him a quick-count pass. Miller rambled 43 yards to the Jaguars’ 30-yard line, setting up the first of four 49ers touchdowns before halftime.

“I was a little too focused on the catch,” Miller said. “I should have been running more to pick up more yards. It was executed great by Kap and the guys in the huddle.”

Meanwhile, Miller’s heart was “pounding” and “going 100 mph” before the snap as he looked to pull off a play the 49ers first attempted to run a year earlier against the Jets, when Kaepernick lined up wide before a timeout was called.

“Yeah, it was pretty smooth,” Miller said half-jokingly. “I wish I was running a little faster at the get-go and not sizing it up.”

Getting tackled by the Jaguars’ safety resulted in Miller getting ribbed by his teammates.

“He got caught,” Goodwin said. “Even though he went 40-something yards, it seemed quick that he got caught.”

To Miller’s credit, his 43-yard reception matched the longest this season by leading wideout Anquan Boldin.

“They gave me a hard time because I looked slow. I don’t know what they expected from me,” Miller joked.

Three years ago, Miller certainly didn’t expect he’d be playing fullback or much less catching passes in the NFL.

He topped out at 265 pounds as a college defensive end, then shed 30 pounds to run the 40-yard dash at 4.5 seconds at his pre-draft pro day.

The 49ers drafted him in the seventh round, and he’s been their starting fullback since his rookie season.

Now weighing 255 pounds, Miller realizes he doesn’t have breakaway speed. More important, he knows that’s what Gore is there for, helping dictate directions at the same time.

“I can kind of hear what he’s saying and figure it out in the play,” Miller said. “Yeah, it moves fast, but you get more chemistry and know what he wants to do.”

Added Gore: “Bruce is smart, so it’s easy with me and him to communicate.”

For more on the 49ers, see Cam Inman’s Hot Read blog at blogs.mercurynews.com/49ers. Follow him on Twitter at twitter.com/CamInman.