Heinicke has also been a member of the New England Patriots, Houston Texans, Carolina Panthers, Washington Football Team / Commanders, and the Atlanta Falcons of the NFL.

In 2020, Heinicke filled in for Washington, to replace an injured Alex Smith, in a playoff game against the Tampa Bay Buccaneers.

Heinicke has been cited as an underdog by teammates, fans, and the media due to his ability to lead teams to wins despite a perceived lack of size and natural arm talent.

Following his senior season, Heinicke was invited to play at the North/South All-Star Football Classic, where he collected 254 yards and three touchdowns en route to MVP honors after helping the North to a 22–0 victory over the South.

He appeared on the reality TV show The Ride, which featured high school quarterbacks competing for a spot in the U.S. Army All-American Bowl.

[7] As a freshman, he led the Monarchs to a 10–3 record in the Colonial Athletic Association (CAA) before losing in the second round of the FCS playoffs against Georgia Southern.

[28] He competed against Mike Kafka to back up Vikings starting quarterback Teddy Bridgewater along with Shaun Hill.

[46] However, he did not see the field during the season and recorded no statistics and had his contract terminated when the league suspended operations in April 2020 due to the COVID-19 pandemic.

[50] He played his first game for the team in Week 16 against the Panthers after starting quarterback Dwayne Haskins was benched in the fourth quarter.

[51] Heinicke started the team's Wild Card Round playoff game against the Tampa Bay Buccaneers after Alex Smith was ruled out due to injury.

[53][54] An impending restricted free agent in 2021, Heinicke signed a two-year, $4.75 million contract extension with the team in February.

[55] In the season opener against the Los Angeles Chargers, he came in to relieve Ryan Fitzpatrick, who left in the second quarter with a hip injury.

[58] In Week 10 against the defending Super Bowl LV champion Buccaneers, Heinicke threw for 256 yards and a touchdown in a 29–19 upset win.

[60] In the Week 14 loss against the Dallas Cowboys, Heinicke left the game in the fourth quarter after getting injured on a sack from defensive tackle Neville Gallimore.

After Wentz was ruled out due to a fractured finger, head coach Ron Rivera named Heinicke as the starting quarterback in Week 7.

[73] On November 1, Falcons head coach Arthur Smith named Heinicke the starting quarterback for the Week 9 game against the Vikings.

[76] Heinicke would be reinstated as the team's starting quarterback for their Week 16 game against the Indianapolis Colts, completing 23 out of 33 passes, throwing for 229 yards and a touchdown with no interceptions in the 29–10 victory.

[77] During the offseason, the Falcons signed Kirk Cousins in free agency and drafted Michael Penix Jr. in the first round, making Heinicke expendable.

On August 28, 2024, the Falcons traded Heinicke to the Los Angeles Chargers in exchange for a conditional seventh-round pick in the 2025 NFL draft.