McDowell was raised in Pasadena, California. He began racing cars at Legion Ascot Speedway in 1934. He later moved on to the independent circuits in the Northwestern United States. He then moved to the CSRA circuit based in Ohio. He had his first experience at the Indianapolis 500 as a riding mechanic for Frank Wearne in 1937. McDowell raced against top midget car drivers at Gilmore Stadium in 1939. He held the points lead until September, and he finished second in the points behind Bob Swanson. He won thirteen features at the track, and is ninth on the track's all-time win list. McDowell finished second in the AAA West Coast midget car points standings in 1947. He also won the 1947 Turkey Night Grand Prix.
McDowell moved to the Midwestern United States in 1948. He won at least eight AAA midget car features, and won the 1948 Soldier Field title.
McDowell competed in the 1949 to 1952 Indianapolis 500 races. He was killed at the Champ Car race at the Milwaukee Mile on June 8, 1952 at age 37.
The Indianapolis 500 was part of the FIA World Championship from 1950 through 1960. Drivers competing at Indy during those years were credited with World Championship points and participation. Johnny McDowell participated in 3 World Championship races but scored no World Championship points.