Ohio State confirmed late Tuesday afternoon that Miller reinjured his throwing shoulder and will need surgery. The two-time Big Ten player of the year left practice in pain Monday after making a short throw.
''My goal is to come back from this injury stronger and better than ever,'' Miller said in a statement.
It's a huge blow to a team considered to be one of the best in the Big Ten and the country, one which already has several major holes to fill on offense.
''My thoughts and prayers are with Braxton and his family,'' Ohio State head coach Urban Meyer said. ''This is an unfortunate injury to a young man who means so much to this program.''
The senior and three-year starter partially tore the labrum in his right shoulder in a loss to Clemson at the Orange Bowl. He had surgery, did not face contact in spring practice and was held out of several practices this month due to soreness.
Redshirt freshman J.T. Barrett is Miller's top backup and will likely be the starter in the Aug. 30 opener against Navy in Baltimore.
Miller said he was on schedule to graduate with a degree in Communications in December and that he also wanted to attend graduate school, ''and then return to lead the Buckeyes next season.''
Miller's options would include taking a medical redshirt and returning to Ohio State for one more season in 2015, or rehabbing the injury and making himself available for the NFL draft in the spring. He toyed with the idea of turning pro last spring but decided against it because of the shoulder surgery might hurt him with pro teams.
With a schedule that includes games at defending Big Ten champion Michigan State on Nov. 8, at Penn State on Oct. 25 and a Sept. 6 date at home against Virginia Tech, the Buckeyes are suddenly confronted by a lot of question marks.
Miller's injury in Monday's practice, first reported by The Columbus Dispatch, came on a routine, unrushed rollout pass. Miller reportedly left the field after screaming in pain but was upbeat later while getting his shoulder iced. He had his arm in a sling on Monday night.
Miller is one of the Big Ten's most decorated quarterbacks, and the falloff in experience compared to his backups is huge.
He has thrown 666 passes in his glittering three-year career, starting as a freshman. Barrett has never played in a game, and sophomore Cardale Jones threw his only two collegiate passes during a 56-0 rout of Purdue.
Miller has also run for 32 touchdowns and passed for 52, putting him in reach of many of Ohio State's career records at his position.
Barrett was an acclaimed four-star recruit out of Wichita Falls, Texas, who watched with Jones last year as Miller took most of the snaps in the Buckeyes' 12-2 season. When Miller was hurt for most of the San Diego State, California and Florida A&M games with a sprained knee, senior Kenny Guiton had big games while leading Ohio State to victories.
The Buckeyes are also replacing four of their five starting offensive linemen, their leading receiver (Corey Brown) and 1,500-yard rusher Carlos Hyde from last year's 11-2 team.
Barrett completed 17 of 33 passes for 151 yards with no interceptions and no touchdowns in Ohio State's annual spring intrasquad scrimmage. Because of Miller's problems with his shoulder, Barrett has gotten a lot of practice time with the Buckeyes' first-team offense in the spring and in recent weeks.
Miller hurt originally hurt his shoulder on the first possession against Clemson in the Orange Bowl, but played the rest of the way in the 40-35 loss. Soon after the injury was discovered, he had surgery in February.
Ohio State said at the time that Miller had ''minor, outpatient surgery.'' But he has had problems with the shoulder since.
Still, he has repeatedly said he would be ready to go in the opener, and did so again between practices on Monday. His workload had been reduced to avoid any ongoing soreness in the arm.
At the Buckeyes' media day, Miller said his arm felt good and he was able to throw as much as he liked.
The injury is perhaps the most crippling at Ohio State since tailback Keith Byars was second to Doug Flutie in the Heisman Trophy race in 1985 but then missed almost all of the following season with a broken bone in his foot.