Johnson played college football for the San Diego Toreros and was selected by the Tampa Bay Buccaneers in the fifth round of the 2008 NFL draft.

Primarily a backup during his career, he has started games for the Buccaneers, Ravens, and Washington Redskins, while also seeing playing time with the Cleveland Browns, Cincinnati Bengals, New York Jets, and San Francisco 49ers.

[4] Johnson attended Oakland Technical High School and was a letterman in football, basketball, and track & field.

Josh Johnson enrolled at University of San Diego in 2004, where he played for the Toreros as a backup quarterback to Todd Mortensen.

Johnson finished the season with 3,256 yards and 36 touchdowns, completing 70.1% of his passes en route to being named team MVP.

Johnson holds the record for the highest career passer efficiency (176.68) in NCAA Division-I football history.

[13] Johnson made his first appearance in a regular season NFL game on September 27, 2009, at Tampa's Raymond James Stadium against the New York Giants.

When Johnson replaced Byron Leftwich as Tampa Bay's quarterback with 9:33 remaining, the Buccaneers had accumulated only 35 total yards and one first down against the favored Giants.

Taking his first pro snap, Johnson found Antonio Bryant for 6 yards, marking the afternoon's first reception by a Tampa Bay wide receiver.

[15] During the 2010 season, Johnson notched a 95.6 passer rating as backup quarterback, and also made appearances in the offense's wildcat formation.

[21] On December 26, 2012, the Cleveland Browns announced they signed Johnson after injuries to Brandon Weeden and Colt McCoy.

[22] After an injury to starter Thad Lewis, Johnson played for one snap in a Week 17 loss to the Pittsburgh Steelers.

[35] On October 2, 2015, Johnson signed with the Indianapolis Colts due to an injury to starter Andrew Luck.

[43] Johnson was active for only two games during the regular season due to injuries to backup quarterback Ryan Nassib.

On December 5, 2018, Johnson signed a one-year contract with the Redskins to be a backup to Mark Sanchez after season-ending injuries to Colt McCoy and Alex Smith.

[59] The following game, on December 22, 2018, Johnson and the Redskins faced the Tennessee Titans in a crucial Week 16 match-up to maintain their playoff hopes.

Despite leading for most of the game, Washington's defense allowed a costly go-ahead touchdown with about four minutes remaining in the fourth quarter.

[65] On November 25, 2019, the Detroit Lions tried to re-sign Johnson but the XFL did not allow him to leave his contract with the Wildcats.

[66] Despite the Wildcats finishing 2–3 in the five-game COVID-19 pandemic shortened season in 2020, Johnson performed admirably in four games (missing Week 1 with an injury)[67] by converting 60 percent of his passes, completing 81 out of 135 attempts for 1,076 yards for 11 touchdowns against only two interceptions for a passer rating of 106.3.

As a result, Johnson was named the highest graded quarterback in the XFL by Pro Football Focus.

[76][77] After starting quarterback Zach Wilson suffered a sprained posterior cruciate ligament in Week 7, Johnson was elevated to the active roster as the second option behind Mike White.

While White was being evaluated for a potential injury in the following week's game against the Bengals, Johnson took the field during the third quarter, his first NFL appearance since 2018.

He completed 2 of 4 passes for 17 yards, setting up a game-tying field goal, before White returned on New York's next possession.

He threw for a career high 317 passing yards and three touchdowns, but was also intercepted on New York's final drive in the 30–45 defeat.

[81] He was forced into the starting role in Week 16 against the Bengals due to Lamar Jackson having an ankle injury and Tyler Huntley testing positive for COVID-19.

[85][86] On October 22, 2022, Johnson was elevated to the team's active roster following an injury to starting quarterback Russell Wilson.

[87] On December 4, 2022, Johnson was signed to the 49ers active roster after a foot injury to quarterback Jimmy Garoppolo.

[94] He was the third-string quarterback behind Lamar Jackson and Tyler Huntley and did not make an appearance during the regular season or postseason.