The team was founded in 1965 with Foyt himself as driver and owner. During the USAC National Championship era the team won three national championships (1967, 1975, and 1979) and two Indianapolis 500s (1967 and 1977), all with Foyt at the wheel. George Snider was among the additional drivers fielded by the team in this period.
During the CART era the team ran partial schedules through most of the 1980s, typically focusing on the three 500-mile races at Indianapolis, Michigan, and Pocono. Foyt himself was the primary driver until a serious crash at Road America in 1990 caused extensive leg injuries requiring lengthy rehabilitation. He returned in 1991 and retired in May 1993. A.J. Foyt Enterprises never won a CART-sanctioned event during its participation from 1979 to 1995; the closest the team came was at the 1995 Bosch Spark Plug Grand Prix, where Eddie Cheever was leading with just over a lap remaining when the car ran out of fuel.
Notable drivers fielded by the team in the CART years included Robby Gordon, who recorded ten top-ten finishes in 1993, and Eddie Cheever, who drove for the team in 1994 and 1995.
The transition to the rival Indy Racing League brought the team its greatest modern success. Scott Sharp won the IRL championship for Foyt in 1996, and Kenny Bräck won the title again in 1998 and added the 1999 Indianapolis 500 victory. These remain the team's most recent championships.
After a difficult period in the mid-2000s, Takuma Sato joined the team in 2013 and gave Foyt its first race win in years at Long Beach. The team expanded to two full-time cars in 2015 with the addition of Jack Hawksworth. In 2017, the team switched from Honda to customer Chevrolet engines after eleven seasons with Honda works support. For the 2021 IndyCar campaign, the team fielded Sebastien Bourdais alongside Dalton Kellett full-time, with Charlie Kimball and J.R. Hildebrand as part-timers for Indianapolis. In 2023, the team entered a technical partnership with Team Penske.
Foyt began fielding NASCAR Cup Series teams in 1973, primarily as a driver himself during the 1970s and 1980s. The team fielded the No. 14 car in Cup racing through the early 2000s with drivers including Ron Hornaday Jr., Stacy Compton, and Larry Foyt, before officially closing the Cup program after an equipment auction in August 2006. The team also competed in the NASCAR Busch Series and Craftsman Truck Series in limited capacity during this period.
With victories across more than five decades and multiple series, A.J. Foyt Enterprises stands as one of IndyCar's institutional teams. The team's championship successes with Sharp and Bräck in the 1990s, and the three national titles won by Foyt himself in the USAC era, mark it as a permanent part of American open-wheel history. The team has fielded more than 70 different drivers across all its racing programs from the 1960s through the 2020s.