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The Arizona Hotshots drafted Wolford with their second-round pick in the 2019 AAF QB Draft. He entered the preseason competing with first-round pick Trevor Knight for the starting job; in the Hotshots' sole preseason game against the Birmingham Iron, Wolford completed 9 of 14 passes for 116 yards, a touchdown, and a two-point conversion. He was named starter prior to the regular season.

On April 10, 2019, Wolford signed with the Los Angeles Rams of the NFL after the AAF suspended operations. He was waived during final roster cuts on August 31, 2019, but was signed the next day to the Rams' practice squad. He signed a reserve/future contract with the Rams on December 31, 2019.

After going undrafted in the 2018 NFL Draft, Wolford signed as an undrafted free agent with the New York Jets. He played in most of the preseason finale against the Philadelphia Eagles, completing 8 passes on 20 attempts for 89 yards and an interception. He was cut from the Jets on September 4.

He had another strong year as a sophomore. In the first game of the season, he threw for a career-high 323 yards in a 41–3 win over Elon; the next week, he threw for 373 yards in a 17–30 loss vs. Syracuse. His 696 passing yards in the first two games constituted the best start ever by a Wake Forest quarterback. As a junior, he started 11 of 13 games, missing one game due to injury.

In the first game of the regular season, a 38–22 win over the Salt Lake Stallions, Wolford completed 18 of 29 passes for 275 yards, four touchdowns, and two two-point conversions; for his performance, he was named Week 1 AAF Offensive Player of the Week. He earned a second Player of the Week award in Week 7, when he completed 15 of 19 passes for 212 yards, two touchdowns, one interception, and a 126.3 passer rating and ran for a 35-yard touchdown in a 32–15 victory against the San Diego Fleet.

As a senior, he had the most impressive season of his college career, earning second-team all-ACC honors and setting school records in single-season passer rating, passing yards, touchdown passes, total offense yards, and touchdowns, as well as the school record in career touchdowns. In the Belk Bowl, set school bowl game records in completions (32), attempts (49), passing yards (400), and touchdowns (4), becoming the first FBS player since 2000 to pass for 400+ yards, rush for 65+ yards, and throw no interceptions in a bowl game.

John Wolford (born October 16, 1995) is an American football quarterback for the Los Angeles Rams of the National Football League (NFL). He played college football at Wake Forest.