The first museum at the Indianapolis Motor Speedway was completed in 1956, designed by C. Wilbur Foster and Associates. It initially displayed Ray Harroun's 1911 Indianapolis 500-winning car and a handful of other vehicles. By 1961, the museum averaged 5,000 visitors per week, not including crowds during the month of May.
In 1975, construction began on a new 96,000-square-foot museum and administration building inside the track’s infield. The expanded museum opened to the public on April 5, 1976, coinciding with the United States Bicentennial celebration. The Indianapolis Motor Speedway was added to the National Register of Historic Places in 1975 and designated a National Historic Landmark in 1987.
In 1993, administrative offices moved to a new building, freeing up floor space within the museum and allowing for an expanded gift shop. The museum parking lot hosted the first “Indy 500 Expo” in 1993, later renamed “Indy 500 FanFest” but discontinued after 1997. In 2016, a revitalization project expanded the museum’s floor space and added interactive displays, and the museum was officially renamed the Indianapolis Motor Speedway Museum. A substantial deaccession process began to refine the collection. In late 2023, the museum closed for the substantial renovations that concluded with the April 2, 2025 reopening.
The museum displays approximately 75 cars at any given time, though the collection contains many more. Exhibits include over thirty Indianapolis 500 winning cars, other Indy cars, pace cars, and passenger cars, with a focus on those manufactured in Indiana. Other items on display include trophies, plaques, helmets, gloves, and driver’s suits.
The museum’s collection includes the 1911 Marmon Wasp, winner of the first Indianapolis 500, driven by Ray Harroun. Other winning cars on display include the 1912 National (Joe Dawson), the 1914 Delage (Rene Thomas), and the 1922 Duesenberg (Jimmy Murphy). The 1939–1940 Boyle Special Maserati, driven by Wilbur Shaw in back-to-back victories, is also part of the collection, as is the 1946 Thorne Engineering (George Robson). The 1947–1948 Blue Crown Spark Plug Special, driven by Mauri Rose in consecutive wins, is also displayed.
Further winning cars include the 1950 Wynn's Offy (Johnnie Parsons), the 1951 Belanger Special (Lee Wallard), and the 1953–1954 Fuel Injection Offy (Bill Vukovich). The 1961 Bowes Seal Fast Offy, driven by A. J. Foyt, and the 1964 Sheraton-Thompson Watson Offy, also driven by A. J. Foyt, are also part of the collection. The 1967 Sheraton-Thompson Coyote Foyt (A. J. Foyt), the 1972 Sunoco McLaren (Mark Donohue), and the 1973 STP Eagle Offy (Gordon Johncock) are also exhibited. The 1977 Gilmore Racing Team Coyote/Foyt (A. J. Foyt), the 1978 First National City Traveler's Checks Lola/Cosworth (Al Unser Sr.), and the 1980 Pennzoil Chapparal (Johnny Rutherford) are also on display.
The museum also displays other significant Indy cars, including the 1912 Fiat driven by Teddy Tetzlaff to second place, and the 1931 Cummins Diesel driven by Dave Evans, the first car to complete the Indianapolis 500 without a pit stop. The 1961 Cooper Climax, driven by Jack Brabham, is also exhibited, as is the 1976 Bryant Heating & Cooling Offy driven by Janet Guthrie during practice, and the 1977 Bryant Heating & Cooling Lightning/Offy driven by Janet Guthrie, the first female to qualify for the Indy 500.
The collection includes at least one Indy 500 pace car from 1911, 1930, 1964, 1966, and 1975 to the present. Passenger cars on display include an 1886 Daimler "Motor Carriage" and an 1886 Benz Patent Motorwagen.
The Indianapolis Motor Speedway Hall of Fame dates back to 1952, established by the American Automobile Association and the Ford Foundation. It was revived in 1961 by Tony Hulman and incorporated into the Speedway museum’s organization. As of 2025, there have been 169 inductees. Candidates are eligible after at least twenty years of participation in professional auto racing. The 2026 inductees will be Scott Dixon and Giampaolo Dallara.