As a sophomore, he was named the starting quarterback before the seventh game against North Carolina State University, after senior Max Browne suffered a season-ending right shoulder injury.

[5] He was platooned during the year and eventually lost the starting position to true freshman Kenny Pickett, for the season finale 24–14 victory against the previously undefeated No.

He led the Dukes to the FCS Championship Game, where the team lost to North Dakota State University.

DiNucci was selected by the Dallas Cowboys in the seventh round (231st overall) of the 2020 NFL draft, after it became apparent that he was considering signing with either the Cleveland Browns or the Chicago Bears if he were to become an undrafted free agent.

[9][8] On October 19, 2020, DiNucci made his NFL debut in relief of Andy Dalton against the Arizona Cardinals.

[11] On October 31, 2020, the Cowboys announced that DiNucci would make his first career start on Sunday Night Football against the Philadelphia Eagles due to Dalton being in concussion protocol.

[12][13] DiNucci completed 21-of-40 passes for 180 yards, lost two fumbles and was sacked 4 times, as the Cowboys lost 23–9 and failed to score a touchdown in back-to-back games, just for the fourth time in franchise history, even though the Cowboys' defense had caused four Eagles' turnovers during the contest.

[14][15] Dinucci was passed on the depth chart by Garrett Gilbert for the backup job for the rest of the season.

[22] On May 16, 2023, DiNucci signed with the Denver Broncos, after participating on a tryout basis at the team's rookie minicamp.

[27] On August 12, 2024, DiNucci signed with the Buffalo Bills after Shane Buechele suffered a neck injury.

[29] On December 10, 2024, DiNucci was signed to the New Orleans Saints' practice squad following an injury to quarterback Derek Carr.