Who Will Win the Backup Quarterback Job for the Cowboys in 2026?

For the seasons prior to 2025, the Dallas Cowboys had a reliable backup option for star quarterback Dak Prescott in Cooper Rush. Rush stepped in when Prescott was hurt and had success, like in 2022, where he led the Cowboys to a 4-1 record as the starter, ultimately finishing his Dallas career with a 9-5 record. Rush's tenure ended in 2025 when he moved to Baltimore, leaving a gap in the backup position until the Cowboys acquired Joe Milton from the New England Patriots in a trade that many did not see coming. While Milton has the upside, Dallas would still sign former Washington quarterback Sam Howell this offseason, which has brought a question many still are wondering: With an offseason, OTAs, and a preseason ahead of the 2026 NFL season, who will win the backup quarterback job in Dallas?

With the start of voluntary training camp for the Cowboys, the one who has been getting the backup reps thus far is Milton. On his first day of practice, he looked solid, notably throwing a touchdown pass on a wheel route to Malik Davis. His style of play and traits are ones that can correlate to him becoming one of the league's best quarterbacks, but what is lacking is the consistency, trust, and ability to put it together in live-action games. Howell's first day of training camp featured a notable touchdown pass to rookie Jordan Hudson with the third team. Unlike Milton, Howell has played several more games and snaps in regular-season action. Howell, in his career as a starter, has a negative record of five wins to 13 losses, but the experience in playing games is there. Both have cases to be and win the backup job in Dallas.

Both players are viable backups, and the decision will likely depend on the state of the season. In the event that Prescott gets injured, the duration of his absence will also be a key factor. If Prescott faces injury early in the year for a short period of time and Dallas needs one of the two, Howell or Milton, to come in and play for a week or two, I believe Howell will play. The experience Howell has gained from playing in numerous NFL games throughout his career, along with his skill in managing the game and making smart decisions on the field, sets him apart from Milton in their competition for what would be the starting job. In the scenario where Dak is sidelined for most of the season and Dallas appears to be out of playoff contention, Milton will likely have the opportunity to start. This situation would provide him with the chance to gain valuable experience as a starting quarterback while also positioning him to compete for the starting job once Prescott retires in the coming years. On the depth chart, Milton will likely be ranked above Howell; however, specific scenarios affecting who can play could lead to both of them starting games for the Cowboys next season if the opportunity presents itself.