Townley began his NASCAR journey in 2008, driving in three Nationwide Series races for RAB Racing. He also competed in seven Craftsman Truck Series events that year for Roush Racing, posting a best finish of 18th. In 2009 he qualified for 26 Nationwide Series races with RAB, finishing 23rd in series points. His aggressive driving style generated controversy from early on, earning him the nickname "John Wrecks Weekly" among fans.
In 2010, Townley joined Richard Childress Racing for the Nationwide Series but was released before the sixth race of the season at Phoenix International Raceway. Clint Bowyer filled the seat for that race, with Bowyer and Morgan Shepherd sharing the car for the remainder of the year. Townley rejoined RAB Racing for a handful of additional starts later that season.
Townley returned to the Camping World Truck Series with RAB Racing in 2012, competing for Rookie of the Year honors. In February of that year, he was arrested on DUI charges following an automobile accident in Oconee County, Georgia, leading to a suspension by the team and NASCAR placing him on probation through year's end. He returned to driving later in March and also attempted his first Sprint Cup Series start at Pocono Raceway with FAS Lane Racing, but was replaced after hitting the wall in practice. That same weekend he recorded his first career top-ten Truck Series finish, placing eighth at Pocono.
For 2013, Townley signed with Red Horse Racing to drive the No. 7 Toyota in the Truck Series. He also competed in ARCA for Venturini Motorsports, winning the season-opening ARCA race at Daytona International Speedway from the pole position. He finished 11th in Truck Series points.
In 2014, Townley drove for Wauters Motorsports in the Truck Series and ran full-time in ARCA for Venturini. Mid-season he moved to Athenian Motorsports, owned by his father Tony Townley, and drove out the remainder of both the Truck and Nationwide Series schedules there.
In 2015, driving the No. 05 for Athenian Motorsports, Townley earned his first and only NASCAR victory at Las Vegas Motor Speedway in the Camping World Truck Series. Leader Matt Crafton pitted for fuel with six laps remaining; Townley stayed out and converted the strategy into the win.
During the 2016 Camping World Truck Series race at Gateway Motorsports Park, Townley was involved in an on-track incident with Spencer Gallagher on lap 154, followed by a physical altercation between the two drivers that drew wide attention and was widely described as one of the more unusual fights in recent motorsport history. NASCAR fined Townley $15,000 and placed him on probation through year's end. He sat out the following race at Kentucky Speedway for concussion treatment, with Parker Kligerman substituting, and later missed the Texas Motor Speedway Truck race for an injured left ankle, with Cody Coughlin filling in.
In January 2017, Townley announced his retirement from motorsports. Athenian Motorsports subsequently ceased operations.
Townley was a native of Watkinsville, Georgia and was named after English clergyman John Wesley. He graduated from North Oconee High School in 2008 and later attended the University of North Georgia. Outside racing, he enjoyed mountain biking, snowboarding, and playing piano, banjo, and guitar.
In 2019, court documents showed Townley was charged with three misdemeanor counts including family violence battery; he pleaded guilty to disorderly conduct and received 12 months probation. He announced his engagement to Laura Bird in late 2016, and in February 2021 he filed for divorce, which was granted in September of that year.
On October 2, 2021, Townley, aged 31, reportedly attacked his former wife Laura Townley and another individual named Zachary Anderson with a hatchet at her home in Athens, Georgia. Anderson shot and killed Townley. Laura Townley was accidentally shot during the incident and sustained serious injuries.