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On March 17, 2020, Thompson signed a two-year contract extension with the Cowboys.

On March 7, 2019, Thompson was re-signed to a one-year contract as an unrestricted free agent. In week 14 against the Chicago Bears on Thursday Night Football, Thompson recorded a team high 11 tackles and sacked quarterback Mitch Trubisky once in the 31–24 loss.

On September 1, 2018, Thompson was waived/injured by the Giants as part of final roster cuts after losing the starting safety job to Curtis Riley.

On October 2, 2018, Thompson was signed to the Arizona Cardinals' practice squad.

On October 9, 2018, Thompson was signed by the Dallas Cowboys off the Cardinals practice squad. He was waived on November 17, 2018, but re-signed three days later. He appeared in 10 games, playing only on special teams.

Thompson entered training camp slated as the starting free safety. Head coach Ben McAdoo officially named Thompson the starting free safety to start the 2017 regular season, alongside strong safety Landon Collins. He started in the New York Giants' season-opener at the Dallas Cowboys and recorded three combined tackles during their 19–3 loss.

On October 8, 2017, Thompson collected a season-high 11 combined tackles (eight solo), two pass deflections, and made his first career interception during a 27–22 loss to the Los Angeles Chargers in Week 5. Thompson made the interception off a pass by Chargers' quarterback Philip Rivers, that was originally intended for wide receiver Keenan Allen, in the third quarter.

On December 4, 2017, the Giants fired head coach Ben McAdoo after they began the season with a 2–10 record. Defensive coordinator Steve Spagnuolo was named the interim head coach for the remainder of the season.

Thompson started in all 16 games in 2017 and recorded 75 combined tackles (61 solo), six pass deflections, and an interception. Pro Football Focus gave Thompson an overall grade of 52.2, which ranked 70th among all qualified safeties in 2017.

Thompson attended the NFL Scouting Combine and completed all of the combine and positional drills. On March 31, 2016, Thompson participated at Boise State's Pro day and attempted to improve his performance in the 40-yard dash (4.58s), 20-yard dash (2.67s), and 10-yard dash (1.59s).

The New York Giants selected Thompson in the third round (71st overall) of the 2016 NFL Draft. Thompson was the sixth safety drafted in 2016.

On June 2, 2016, the New York Giants signed Thompson to a four-year, $3.45 million contract that includes a signing bonus of $837,136.

He made his professional regular season debut in the New York Giants' season-opener at the Dallas Cowboys and made three combined tackles in their 20–19 victory. On September 18, 2016, Thompson earned his first career start after he surpassed Nat Berhe on the depth chart and was named the starting free safety. He made a season-high four solo tackles before exiting in the fourth quarter of the Giants' 16–13 win against the New Orleans Saints due to a foot injury. Defensive coordinator Steve Spagnuolo was impressed with Thompson's mastery of defensive schemes and his ability to get his teammates lined up correctly.

On November 9, 2016, the New York Giants placed Thompson on injured reserve after he missed six games (Weeks 3–9) due to his foot injury that required surgery. Thompson finished his rookie season in 2016 with seven combined tackles (six solo) in two games and one start.

During his senior year in 2015, Thompson tied Eric Weddle's Mountain West Conference record for career interceptions. Later in the same season, in a game against UNLV, Thompson recorded his 19th interception of his career breaking the mark set by Weddle.

Thompson again started all 13 games as a junior in 2014. He recorded 71 tackles and seven interceptions and was named a second team All-American by CBSSports.com.

As a sophomore in 2013, he started all 13 games and recorded 63 tackles and four interceptions.

After redshirting his first year at Boise State in 2011, Thompson appeared in all 13 games, with six starts, as a redshirt freshman in 2012. For the season he had 43 tackles and three interceptions.

Darian Thompson (born September 22, 1993) is an American football safety for the Dallas Cowboys of the National Football League (NFL). He played college football at Boise State.