Industrialist Alexandre Lamblin commissioned engineer René Jamin to design the 2.548-kilometre oval-shaped track to accommodate vehicles of up to 1,000 kg at 220 km/h (140 mph). The circuit's defining feature was its exceptionally steep banking, designed to allow cars to maintain high speeds through the turns without needing to reduce pace significantly. A road circuit was added to the facility in 1925, creating the combined configuration used for Grand Prix racing.
The circuit's first major race was the 1925 French Grand Prix, held on 26 July 1925 and organised by the Automobile Club de France. Robert Benoist won in a Delage, but the race was marked by the fatal crash of Antonio Ascari, whose Alfa Romeo P2 left the track and struck a tree. Ascari was the reigning European champion at the time.
The circuit hosted the French Grand Prix again in 1927 and then each year from 1931 to 1937, making it one of the primary venues for the French round of the pre-war Grand Prix calendar. In 1929, Hellé Nice drove an Oméga-Six to victory in the all-female Grand Prix held at Montlhéry as part of the Journée Feminine programme.
In July 1926 Violette Cordery led a team that drove an Invicta at an average speed of 113.8 km/h over 8,047 kilometres (5,000 miles), a performance recognised by the Dewar Trophy of the Royal Automobile Club, making Cordery the first woman to receive that award.
In 1939 the track was sold to the French government, which provided no maintenance during the war years. In December 1946 it was again sold, this time to the Union technique de l'automobile et du cycle (Utac), which has operated it ever since as a vehicle testing and certification facility. The last certification for racing events was obtained in 2001, and the circuit is no longer used for contemporary competition.
Montlhéry hosted significant motorcycle competition in addition to its car racing calendar. The Grand Prix de France was organised at the circuit in 1925, 1931, 1935, and 1937. The Bol d'Or, France's premier 24-hour motorcycle endurance race, was held at Montlhéry before World War II from 1937 to 1939 and returned there after the war from 1949 to 1960 and again in 1969 and 1970. British motorcycles dominated the post-war Bol d'Or at Montlhéry, with Norton, Velocette, and Triumph machinery taking the majority of victories. French racer Gustave Lefèvre won seven editions of the post-war Bol d'Or at the circuit aboard a Norton Manx, riding solo for all 24 hours in at least some of those attempts, holding the record with an average speed of 107 km/h in 1953.
In 1961 a team of eight riders from British manufacturer Veloce, including the company's managing director, used a near-standard Velocette Venom Clubman machine to cover the circuit at over 100 mph (100.06 mph exactly) for 24 consecutive hours, setting a world record for a 500cc motorcycle that still stands.
In 1933 the circuit hosted the UCI Road World Championships for cycling. The 2010 Ken Block Gymkhana Three promotional video was filmed at the facility's speed ring.
Montlhéry represents an important early example of a permanent purpose-built speed circuit in continental Europe, constructed at a period when France was the dominant force in Grand Prix racing and when high-speed oval testing remained closely linked to Grand Prix competition. The circuit's role as the venue for the 1925 French Grand Prix, at which Antonio Ascari died, gave it a place in the founding narrative of European motorsport safety consciousness. Today the Autodrome operates primarily as a testing and homologation facility for Utac, which conducts vehicle certification work on behalf of automotive manufacturers and regulatory bodies.