Cherkassky was born in Odessa, Ukraine on October 7, 1909 (but frequently given as 1911), the son of a Jewish family. Cherkassky's father was a dentist, and his mother a professional pianist, with whom he began piano studies at the age of four.

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Cherkassky's debut in his native city in 1920 was sensational. In December 1922, the family moved to the United States, settling first in Baltimore, Maryland. At this time the family gave Cherkassky's birth date as 1911, believing that a prodigy of 12 would be regarded as more remarkable than an adolescent of 14.

After consulting famous pianists of the day (Vladimir de Pachman, Sergei Rachmaninoff, Ignace Jan Paderewski, and Josef Hofmann), Cherkassky's parents enrolled him in the newly opened Curtis Institute of Music in Philadelphia in the fall of 1925. He began formal studies with Hofmann, with whom he would study until 1935, becoming his most successful student. He also studied briefly with David Saperton, another member of the Curtis faculty.

Cherkassky's American debut took place in March of 1923 in Baltimore. His playing was described as supernatural, and at the age of fourteen he was invited to play for President Harding at the White House.

His subsequent appearances took him to New York City (formal debut in November 1924), Boston, Philadelphia, and abroad. As a young man he performed in Australia, New Zealand, South Africa, England, Germany, Russia, Japan, and China.

Cherkassky early earned a reputation for spontaneity, creativity, and technical perfection in his playing. His sound was unique and became almost instantly recognizable. He was famous for never playing the same piece the same way.

In addition to the standard virtuoso repertoire, especially Chopin, Liszt, and Rachmaninoff, Cherkassky also performed works by Hofmann, Paul Hindemith, Morton Gould, Benjamin Britten, Luciano Berio, Alban Berg, and other twentieth-century composers.

He recorded for Nimbus, Decca, HMV, Orfeo, Biddulph, RCA Victor, and other major companies.

Following negative reviews of his recitals in New York in 1940, Cherkassky's career slowed down.

During World War II, Cherkassky lived with his mother in Los Angeles. He described the war years as the worst time of his life. Although he did some film work during these years, concert engagements were rare. His career did not recover until a very successful tour of Scandinavia in 1946.