He played college football at Itawamba before transferring to Mississippi State and was selected by the Detroit Lions in the second round of the 2013 NFL draft.

[1] He was named All-State by The Atlanta Journal-Constitution at defensive back following his senior season, and was also chosen for the Georgia North-South All-Star Game.

[3] As a freshman at ICC, Slay earned First-team Mississippi Association of Community and Junior Colleges (MACJC) All-State and National Junior College Athletic Association (NJCAA) All-Region 23 honors after record 41 tackles, 3 tackles for loss, 1 sack and forced two fumbles after only playing five games for Coach Jon Williams and the Indians.

[13] Head coach Jim Schwartz named Slay the starting cornerback to begin his rookie season.

[17] On December 31, 2013, the Detroit Lions fired head coach Jim Schwartz after they failed to qualify for the playoffs and finished with a 7–9 record in 2013.

[16] Slay entered training camp slated as a starting cornerback, along with Rashean Mathis, but saw minor competition from Chris Houston.

Head coach Jim Caldwell named Slay and Rashean Mathis the starting cornerbacks to begin the regular season in 2014.

[19] Slay started the season-opener against the New York Giants and recorded three solo tackles and a season-high three pass deflections in a 35–14 victory.

On September 28, 2014, Slay recorded five combined tackles, deflected a pass, and made his first career interception during a 24–17 victory at the New York Jets in Week 4.

Slay made his first career interception off a pass by quarterback Geno Smith, that was originally intended for wide receiver Eric Decker, and returned it for a 40-yard gain in the fourth quarter.

On December 14, 2014, Slay recorded five combined tackles, deflected two passes, and made an interception during the Lions' 16–14 win against the Vikings in Week 15.

Slay intercepted a pass by Vikings' quarterback Teddy Bridgewater, that was intended for wide receiver Greg Jennings, in the second quarter.

[25] On December 13, 2015, he recorded two solo tackles, deflected a pass, and intercepted St. Louis Rams quarterback Case Keenum during a 14–21 loss.

Head coach Jim Caldwell named Slay and Nevin Lawson the starting cornerbacks in 2016, along with nickelback Quandre Diggs.

[28] On October 2, 2016, Slay recorded four solo tackles, a season-high three pass deflections, and made his first career sack during the Lions' 17–14 loss at the Bears in Week 4.

[29] In Week 7, Slay recorded two combined tackles before exiting the Lions' 20–17 victory against the Redskins in the third quarter due to a hamstring injury.

[32] He finished the 2016 season with 44 combined tackles (43 solo), 13 passes defensed, two interceptions, a sack, and a forced fumble in 13 games and 13 starts.

On January 7, 2017, Slay recorded two combined tackles in the Lions' 26–6 loss at the Seattle Seahawks in the NFC Wildcard Game.

[49] During Slay's week 8 homecoming game against the Lions, he recovered a fumble by D'Andre Swift and returned it for a 33-yard touchdown in the 44–6 win.

[54] Slay reached his first career Super Bowl when the Eagles defeated the San Francisco 49ers in the NFC Championship Game.

[60] Slay has continued using the nickname during his NFL career,[61] including referring to himself as such in player introductions during national telecasts,[62] and hosts a weekly in-season podcast of the same name.