Opper's artistic evolution saw a shift from abstract gestural works influenced by nature to a refined, pure form of abstraction. He believed that art should transcend mere representation to evoke profound aesthetic experiences. His association with prominent artists such as Milton Avery, Adolph Gottlieb, and Mark Rothko enriched his creative approach. Throughout the 1940s and 1950s, Opper balanced teaching positions across the United States with his artistic pursuits, eventually settling into the purely abstract style that won him critical acclaim.
John Opper's legacy is preserved in prestigious museum collections, including the Museum of Modern Art, the Whitney Museum of American Art, and the Metropolitan Museum of Art, all in New York, New York. He was also the recipient of numerous award, such as a Guggenheim Fellowship and the Jimmy Ernst Award from the American Academy of Arts and Letters.