On April 25, 2010, the Dallas Cowboys signed Church to a three-year, $1.22 million contract that includes a $3,500 signing bonus after he went undrafted during the 2010 NFL Draft.

He made his professional regular season debut in the Dallas Cowboys’ Week 2 matchup against the Chicago Bears after being inactive for their season-opener. Church finished the Cowboys’ 27–20 loss with one assisted tackle. He made his first career tackle with teammate Danny McCray on Danieal Manning during a 21-yard kick return by Manning in the second quarter. On October 31, 2010, Church collected a season-high four combined tackles in the Cowboys’ 35–17 loss to the Jacksonville Jaguars. On November 9, 2010, the Dallas Cowboys fired head coach Wade Phillips after a 45–7 loss to the Green Bay Packers and falling to a 1-7 record. He finished his rookie season in 2010 with 20 combined tackles (15 solo) in 15 games and zero starts. He finished fourth on the team with 16 tackles on special teams.

Church returned to training camp in 2011 and competed for a role as a backup safety against Andrew Sendejo, Danny McCray, Akwasi Owusu-Ansah, and Michael Hamlin. Head coach Jason Garrett named him the backup behind Gerald Sensabaugh and Abram Elam to start the regular season.

In Week 4, Church recorded a season-high six combined tackles in a 34–30 loss to the Detroit Lions. On December 11, 2011, he earned his first career start and recorded two solo tackles before leaving the Cowboys’ 37–34 loss to the New York Giants in the third quarter with a shoulder injury. On December 13, 2011, the Dallas Cowboys placed Church on injured reserve after discovering his shoulder would require surgery to repair the AC joint. He finished his second season in 2011 with 28 combined tackles (21 solo) in 13 games and one start.

He started the Dallas Cowboys’ season-opener at the New York Giants and recorded two combined tackles in their 24–17 victory. On September 23, 2012, Church made a season-high three solo tackles in a 16–10 victory against the Tampa Bay Buccaneers, but left in the third quarter after sustaining a torn achilles. He underwent surgery to repair the tendon two days later. Church finished his last season under defensive coordinator Rob Ryan with six combined tackles (four solo) in three games and three starts.

Still rehabbing from a serious injury, the Cowboys took a gamble that he would make a full recovery and on October 26, 2012, signed Church to a four-year, $8.82 million contract extension that included $3.32 million guaranteed and a signing bonus of $2.5 million.

On October 20, 2013, Church recorded five combined tackles, broke up a pass, and made his first career interception off quarterback Matt Barkley during a 17–3 victory at the Philadelphia Eagles. In Week 10, he collected a season-high 14 combined tackles (nine solo) in the Cowboys’ 49–17 loss to the New Orleans Saints. The following week, Church made 13 combined tackles (eight solo) in a 24-21 victory at the New York Giants. When injuries impacted the depth at linebacker, he also provided help by playing linebacker on passing situations. Church finished his first full season as a starter leading the team with 147 combined tackles (107 solo), six pass deflections, three forced fumbles (led the team), and an interception in 16 starts.

The Dallas Cowboys finished first in the NFC East with a 12–4 record and received a playoff berth. On January 4, 2015, Church started in his first career playoff game and recorded four combined tackles during a 24–20 victory against the Detroit Lions in the NFC Wildcard Game. The following week, he made eight combined tackles in the Cowboys’ 26–21 loss at the Green Bay Packers.

In Week 10, Church collected a season-high 11 combined tackles (nine solo) during the Cowboys’ 10–6 loss at the Tampa Bay Buccaneers. On December 13, 2015, he tied his season-high of 11 combined tackles (nine solo) during a 28–7 loss at the Green Bay Packers. On December 27, 2015, Church recorded seven combined tackles, but left the Cowboys’ 16–6 loss at the Buffalo Bills in the fourth quarter after breaking his right arm. He was expected to be in a cast for 6–8 weeks and missed the last game of the season. He finished second on the team with 136 combined tackles (78 solo) and a forced fumble in 15 starts.

During Week 2, Church made five combined tackles, broke up a pass, and intercepted a pass by Kirk Cousins in the endzone. The interception set up the Cowboys’ game-winning drive in their 27–23 victory at the Washington Redskins. Against the Green Bay Packers he had five tackles, a forced fumble, a pass defended, and a third-quarter interception. On October 30, 2016, Church made three combined tackles before leaving Dallas’ 29–23 victory against the Philadelphia Eagles in the third quarter after fracturing his forearm during a touchdown drive by the Eagles. He was sidelined for four consecutive games (Weeks 9–12) due to the injury, but returned in Week 13 and opted to play with a cast on.

In Week 16, he collected a season-high 12 combined tackles (seven solo) in a 42–21 victory against the Detroit Lions. Church completed the 2016 season with 85 combined tackles (61 solo), four passes defended, and two interceptions in 12 games and 12 starts. He received an overall grade of 86.2 from Pro Football Focus in 2016 and ranked ninth among all qualifying safeties. In the Divisional Round against the Green Bay Packers, Church made four combined tackles and made his first career sack on Aaron Rodgers as the Cowboys lost by a score of 34-31.

On March 9, 2017, the Jacksonville Jaguars signed Church to a four-year, $26 million contract that includes $12 million guaranteed. Head coach Doug Marrone named Church the starting strong safety, along with free safety Tashaun Gipson, after it was left vacant due to Johnathan Cyprien’s departure to the Tennessee Titans in free agency.

In Week 4, Church made six combined tackles and sacked quarterback Josh McCown in the Jaguars’ 23–20 loss at the New York Jets. On October 8, 2017, Church recorded five combined tackles, deflected a pass, and returned an interception by Ben Roethlisberger for a 51-yard touchdown during a 30–9 victory at the Pittsburgh Steelers. It marked his second touchdown in eight seasons. The Jaguars’ defense set a franchise record by intercepting five passes by Ben Roethlisberger during their game. In Week 12, he collected a season-high nine combined tackles, broke up a pass, and intercepted a pass by Carson Palmer during a 27–24 loss at the Arizona Cardinals. Church finished his first season with the Jacksonville Jaguars with 72 combined tackles (58 solo), eight pass deflections, four interceptions, 1.5 sacks, and a touchdown in 16 starts.

The Jaguars finished atop the AFC South with a 10–6 record to clinch a playoff berth. The Jaguars defeated the Buffalo Bills in the AFC Wildcard Game and went on to narrowly defeat the Steelers 45–42 in the AFC Divisional round. Church recorded seven combined tackles during their victory over the Steelers. On January 21, 2018, Church made a tackle during the Jaguars’ 24–20 loss on the road against the New England Patriots. He drew criticism and received a personal foul after delivering a hit to tight end Rob Gronkowski’s head during the second quarter. Gronkowski was immediately carted off the field and did not return after he suffered a concussion. On January 26, 2018, Church was fined $24,309 for the hit. Pro Football Focus gave Church an overall grade of 83.2 in 2017, ranking him 22nd among all qualifying safeties.