In 1926, Crawford composed her Sonata for Violin and Piano; performed at modern music concerts in the late '20s, it prompted a critic to remark that Crawford could "sling dissonances like a man." She was recognized early on as a woman composer who did not fit the sentimental stereotypes associated with the standard profile. In Chicago, Crawford joined the circle of Djana Lavoie Herz, pianist and ex-follower of Scriabin; through Herz she met Dane Rudyhar, Henry Cowell, and pianist Richard Bühlig. Cowell quickly became a supporter of Crawford's work, arranging for performances of her music in New York and publishing it in the periodical New Music Quarterly. Crawford worked as a piano teacher for the children of poet Carl Sandburg; it was he who first interested her in American folk songs. She contributed arrangements to his 1927 book The American Songbag, and later created significant original settings to eight of his poems.
By 1930, Ruth Crawford was a force to be reckoned with in American modernism. Stylistically, her work stood out in its uncompromising use of dissonance, contrapuntal ostinati, striking choice of texts and tidy formal construction. In March 1930, Crawford won a Guggenheim Fellowship to travel to Europe; the first woman so honored. In Berlin, Crawford composed Three Chants set to a wordless text for women's chorus; this eerie, experimental work has no obvious parallels to any music written before the 1960s. The following year witnessed her most famous work, String Quartet 1931, and with its publication Crawford provided the definitive foil to the old maxim that women "just can't write" classical music with the strength and seriousness of male composers.
In 1929, she began study with Charles Seeger, a key figure in American music as a composer, theorist and musicologist. They married in 1932. She likewise adopted several of Seeger's theoretical methods that mark the works of her most productive period, 1930-1933; however, her composing came to a virtual standstill around 1934. Among her children with Seeger were daughter Peggy and son Mike, both to become renowned folk singers and teachers in adulthood. In 1936, the Seegers moved to Washington, D.C., to work in folk song collecting for the Library of Congress. Crawford acted as transcriber for the book Our Singing Country and, with Charles Seeger, for Folk Song USA, both authored by John and Alan Lomax. As Ruth Crawford Seeger she published her own pioneering collection, American Folk Songs for Children, in 1948, designed for use in elementary grades. This and the other "Crawford Seeger" books are regarded as key texts in primary music education, and were widely adopted and imitated in the field. Crawford only returned to serious composition with the Suite for Wind Quintet in 1952. By the time it was completed, she learned she had cancer. Ruth Crawford died at the age of 52.