Farris was selected by the San Diego Chargers of the American Football League (AFL) in the 17th round (136th overall) of the 1964 AFL draft with a future draft pick, which allowed the team to draft him before his college eligibility was over.[16][17] He was also selected by the Los Angeles Rams of the National Football League (NFL) in the 11th round (147th overall) of the 1964 NFL draft.[16] Despite "weighing attractive offers" from the Rams,[2] it was announced on December 2, 1964, that Farris had signed with the Chargers.[18] He received praise from head coach Sid Gillman, who said a few weeks later that San Diego "got a splendid guard in John Farris".[19] Farris was one of a record 38 rookies who reported to training camp in July 1965.[20][21] Within a few days, he was highlighted as the "best-looking rookie" in camp by the Daily Times-Advocate, who reported that "the entire staff was enthused about [his] play".[22] Farris was the only rookie tabbed as a starter in the team's first intra-squad scrimmage on July 24, opening at left guard ahead of regular Pat Shea.[23][24] He missed the second team scrimmage the following week after suffering a badly sprained right wrist,[25][26] but was back in time for their first preseason game against the Oakland Raiders.[27]
As a rookie in 1965, Farris appeared in all 14 games for San Diego as a reserve left guard,[28] though he was mostly used on special teams.[4] He credited teammate Ernie Ladd with helping him improve his line play, even choosing to block the then-315 lb (143 kg) defensive tackle on pass drills during the preseason.[29] In a game against the New York Jets in October, Farris recovered a fumble in the red zone on a punt return by Kern Carson midway through the fourth quarter, setting up a field goal in an eventual 34–9 win.[30] The Chargers captured the AFL Western Division title after finishing the season with a 9–2–3 record and lost to the Buffalo Bills in the AFL Championship Game by a score of 23–0.[31] Farris was initially ruled out of the title game due to a strained knee,[32] but he recovered and was able to play in the only playoff game of his career.[33][34]
"Bulk and mobility are necessities for a good pass blocker. If you don't have those two things, the big tackles will just pick you up and wheel you back like you're on roller skates." – Farris in 1966[35]
In 1966, Farris again appeared in all 14 games for San Diego as a left guard,[28] serving in a backup role behind starter Ed Mitchell.[36][37] The Chargers went 7–6–1 and failed to qualify for the playoffs.[38] On April 25, 1967, Farris was traded to the Miami Dolphins for defensive back John McGeever.[39] He was one of 27 veterans who were ordered by Miami head coach George Wilson to report to training camp a week early along with the rookies.[40] However, Farris never showed up to camp,[41] and was subsequently released.[28] According to Wilson: "We've never heard from Farris and [Bob] Petrich said he heard he was talking of joining the Peace Corps."[41]