[5] On January 21, 2017, Hairston recorded three combined tackles as part of the East team that lost 10–3 to the West in the 2017 East-West Shrine Game.

[12][13] Head coach Chuck Pagano named Hairston the fourth cornerback on the Colts' depth chart to begin the regular season in 2017.

The following week, Hairston made his first career start as a nickelback after Vontae Davis was ruled inactive due to a groin injury.

On October 1, 2017, Hairston collected a season-high six combined tackles and forced a safety for the first scoring play of his career during a 46–18 loss at the Seattle Seahawks in Week 4.

He made his first career interception off a pass by Titans' quarterback Marcus Mariota, that was originally intended for wide receiver Taywan Taylor, and returned it for a ten-yard gain in the second quarter.

[19] He finished his rookie season in 2017 with 36 combined tackles (25 solo), five pass deflections, two sacks, one interception, and a safety in 14 games and four starts.

[22] Hairston competed against Kenny Moore II and Pierre Desir to be a starting cornerback to begin the regular season.

[23] Head coach Frank Reich named Hairston a starting cornerback to begin the regular season, alongside Kenny Moore and safeties Malik Hooker and Clayton Geathers.

[24][25] Hairston was inactive for the Colts' Week 5 loss at the New England Patriots on Thursday Night Football due to a hamstring injury.