The founder of Papa John's, John Schnatter, began his pizza career at Rocky's Sub Pub in Jeffersonville, Indiana while attending Jeffersonville High School. John graduated from Jeffersonville High in 1980, and continued his association with the pizza business while attending Ball State University, working as a delivery driver for Greek's Pizzeria in Muncie. Upon graduating, he began working for his father, who was co-owner of the bar Mick's Lounge in Jeffersonville. In 1983, he sold his car (a 1971 Chevrolet Camaro Z28) to buy out the other owner of the bar, and started serving pizza to customers. Business started picking up.

In 2009, with the pizzeria chain firmly established, Schnatter set out to find his beloved '71 Camaro. After a few months, the original buyers of the car saw Schnatter mention his search for the car in a TV interview. They had sold the car only five years prior for $4,000 to Jeffrey Robinson of Flatwoods, Ky., who collected the $250,000 reward for returning it to Schnatter. The buyers Schnatter had sold the car to in 1983 were paid a $25,000 finder's fee.

The corporation credits its growth to great customer service, quality products, and menu simplicity, in contrast with other chains' focus on low prices. Fewer options in crust styles and side dishes simplify inventory management and are meant to allow greater focus on what options there are. However, since the mid-1990s, Papa John's has followed the industry trend and greatly expanded its menu options, adding thin-crust, pan pizza, and whole wheat crust options (available in one size only); "Robusto", barbecue, and Alfredo; 10 specialty pizzas, many with new toppings and new cheeses; chicken strips and three flavors of chicken wings; many dessert pastries, such as Apple pie; and new variations of bread sticks and cheese sticks.

The thin crust has been advertised as crispier than others (similar to St. Louis-style pizza) and the "Robusto" sauce introduced with the pan crust has chunky tomato pieces and more vibrant spice notes. To simplify in-store operations and to provide product consistency between stores, many functions such as dough production are carried out by an off-site commissary system similar to that of most other fast food chains.