[4][5] Throughout training camp, Littleton competed for a roster spot as a backup outside linebacker against Josh Forrest, Cameron Lynch, Ian Seau, and Matthew Wells.

[6] Head coach Jeff Fisher named Littleton a backup outside linebacker to begin the regular season, behind Akeem Ayers and Mark Barron.

On January 13, 2017, the Rams announced their decision to hire Washington Redskins' offensive coordinator Sean McVay as their new head coach.

Head coach Sean McVay named Littleton a backup inside linebacker to begin the season, behind Mark Barron and Alec Ogletree.

During Week 16, he recorded seven combined tackles, deflected a pass, made his first NFL sack and interception during a 27–23 road victory against the Tennessee Titans.

[14] Littleton finished the season with 36 combined tackles (22 solo), four pass deflections, one sack, and one interception in 16 games and four starts.

Littleton entered training camp slated as a starting inside linebacker after Ogletree was traded to the New York Giants.

[16] Littleton started in the season-opener against the Oakland Raiders and recorded 13 combined tackles (11 solo), broke up a pass, and made an interception in a 33–13 road victory.

[17] Two weeks later against the Los Angeles Chargers, he had 10 combined tackles (5 solo), a pass deflection, and blocked a punt in the end zone that was recovered by Blake Countess for a touchdown in a 35–23 win.

Head coach Sean McVay said, "Can't really understate what a great job and what an impact Cory Littleton's made."

The Rams reached Super Bowl LIII and lost 13–3 to the Patriots, while Littleton recorded 10 tackles, two passes defended, and an interception.