Cowboys post-draft roster review: Quarterbacks

The Cowboys quarterback room is going to look very different this season.

With the NFL draft completed and the Dallas Cowboys having signed their undrafted rookie free agents following the draft, the 2025 edition of the team is starting to round into shape. We can fairly assume that what Dallas has currently is what they’ll go with for most of the summer heading into the season. Also, there have been some exciting additions to the team that will surely have intrigue throughout the remainder of the offseason.

The Cowboys held a rookie minicamp before the full team reconvenes at mandatory minicamp starting June 10th. There’s a lot of ground to cover in examining this team before the season begins. In our first installment of the Cowboys’ roster series, we examine the team’s signal-callers, the quarterbacks.

Dak Prescott

This season Dak Prescott makes his return after suffering a season-ending hamstring injury. Prescott was heading into last season coming off of one the best seasons of his career when he threw for 4,516 yards and 36 touchdowns versus only nine interceptions, resulting in an All-Pro selection. Recently, Prescott looks to be in great shape. However, there’s a bit of concern about how Prescott looked before suffering his injury. Prescott had a career-low passer rating and was inconsistent in the eight games he was active.

Of course, the big question is – Can Prescott deliver in the postseason? Prescott is closing in on franchise passing records but the main goal eluding him and the team is making it to an NFC conference championship appearance, they are the only NFC team to not have accomplished that since 1995. After being handsomely rewarded with a four-year, $240M contract, Prescott is the leader of the team for the foreseeable future. However, everything hinges on him remaining healthy.

Joe Milton

With Trey Lance and Cooper Rush leaving the team, the Cowboys had a significant need for a backup quarterback. Rush had started 14 games for the Cowboys, winning nine of them. Therefore, getting someone capable of holding down the fort should Prescott get injured again was of the utmost importance. The Cowboys went with a trade for Joe Milton from the New England Patriots. Dallas engineered a late-round pick swap to acquire Milton who provides the Cowboys with enticing upside and contractual control over the next three years.

Milton is a terrific athlete with very good mobility. He’s got an explosive arm with premier velocity to drive the ball down the field with ease. Some draftniks opined that Milton had the strongest arm in the 2024 draft class. As exciting as he is, is a very raw prospect that will need time to develop. Yet, at times Milton can make plays akin to Josh Allen. The Patriots had a market for him but ultimately traded him for fairly cheap trade capital to the Cowboys. Milton wanted to be in Dallas and the Cowboys are happy to have him. The health of Dak Prescott is most important, but Milton certainly has characteristics you covet in a backup.

Will Grier

Having Will Grier back on the team is somewhat of a full-circle moment. Grier played arguably the game of his career during the preseason finale in 2023 where he threw for 305 yards and two passing touchdowns with Prescott calling plays for him. This came on the heels of the team informing Grier that he would be released to make room on the roster for the acquisition of Trey Lance from the San Francisco 49ers. Surely Grier will have extensive time in the preseason and it’s possible he could initially be the team’s backup coming out of training camp ahead of Milton if he has a strong summer. Like Milton, Grier has little experience having started only two regular seasons. Grier has a lot of moxie and deceptive mobility at quarterback. However, if he has an uneven preseason, he is likely bound for the practice squad, but not a bad alternative for the Cowboys considering Grier has at least shown flashes in a small sample.