[7] Throughout training camp, Brown competed to be a backup cornerback against Josh Thomas, Isaiah Frey, Dax Swanson, and Deji Olatoye.

[8][9] Head coach Jason Garrett named Brown the fourth cornerback on the depth chart to start the regular season.

On September 25, 2016, Brown earned his first career start in place of Orlando Scandrick who was inactive due to a hamstring injury.

[12] On December 11, 2016, Brown recorded two solo tackles, broke up a pass, and made his first career interception as the Cowboys lost 10–7 at the New York Giants in Week 14.

Brown intercepted a pass attempt by Giants’ quarterback Eli Manning, that was originally intended for wide receiver Victor Cruz in the fourth quarter.

Brown entered training camp as a possible candidate to win the role as a starting cornerback after Brandon Carr departed in free agency.

Head coach Jason Garrett named Brown the fourth cornerback on the depth chart to begin the regular season, behind Orlando Scandrick, Nolan Carroll, and Chidobe Awuzie.

[18] On December 31, 2017, Brown recorded six combined tackles, deflected a pass, and made his first career sack in the Cowboys’ 6–0 win at the Philadelphia Eagles in Week 17.

[19] Brown finished the 2017 NFL season with 56 combined tackles (47 solo), 11 pass deflections, two interceptions, and a sack in 16 games and ten starts.

[20] Head coach Jason Garrett named Brown the third cornerback and first-team nickelback on the Cowboys’ depth chart to begin the regular season.

[28] In Week 5 against the Giants, Brown returned a fumble forced by teammate DeMarcus Lawrence on Daniel Jones for a 29-yard touchdown during the 37–34 win.

[29] In Week 15 against the San Francisco 49ers, Brown recorded his first interception of the season off a pass thrown by Nick Mullens during the 41–33 win.

[30] Brown was named the starter at right cornerback, helping fill the void left by Chidobe Awuzie's departure in free agency.