He drove in the AAA Championship Car series in the 1949 and 1950 seasons with 4 starts, including the 1950 Indianapolis 500. He finished in the top ten once, in 6th position at Milwaukee in 1950.

In 1951, he moved to NASCAR, where he was a very successful Grand National driver through 1955.

In 1956, he returned to the USAC Championship Car series, racing in the 1956–1964 seasons with an additional 41 starts, including the Indianapolis 500 races in 1956 and 1958-1964. He finished in the top ten 21 more times, with his best finish in 2nd position in 1959 at Daytona.

Dick sat on the pole for the 1958 Indianapolis 500. On the first lap, he and fellow front-row starter Ed Elisian raced into turn 3 and started a chain-reaction accident which involved 15 cars and cost the life of Pat O'Connor. With that accident, Rathmann became the first Indy pole-sitter to complete no laps. This feat has been repeated only twice in Indy history, first by Roberto Guerrero and then by Scott Sharp.

Dick was the elder brother of 1960 Indianapolis 500 winner Jim Rathmann. Jim and Dick switched names in 1946 so that his younger brother could enter a race while underage. For what was supposed to be a short time, he adopted the name "Dick" and his brother adopted the name "Jim." The name change stuck for life.

In 2009, Rathmann was inducted into the .

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. Dick Rathmann participated in 5 World Championship races. He started on the pole once and accumulated a total of 2 World Championship points.

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