"[10] Rushing was inspired to pursue music and sing blues by his uncle Wesley Manning and George "Fathead" Thomas of McKinney's Cotton Pickers.

[11] Rushing toured the Midwest and California as an itinerant blues singer in the early 1920s before moving to Los Angeles, where he played piano and sang with Jelly Roll Morton.

[13] Due to his tutelage under his mentor Moten, Rushing was a proponent of the Kansas City, Missouri, jump blues tradition exemplified by his performances of "Sent for You Yesterday" and "Boogie Woogie" for the Count Basie Orchestra.

[15] He appeared in the 1957 television special Sound of Jazz, singing one of his signature songs, "I Left My Baby", backed by many of his former Basie band members.

In 1958, he was among the musicians included in an Esquire magazine photo by Art Kane that was memorialized in the documentary film A Great Day in Harlem.

Whitney Balliett, jazz critic for The New Yorker, wrote of Rushing that, "His supple, rich voice and his elegant accent have the curious effect of making the typical roughhouse blues lyric seem like a song by Noël Coward".

[22] The critic Nat Hentoff, who ranked Rushing as one of the "greatest blues singers," credited him as a seminal influence in the development of post–World War II popular black music.

"[24] In an essay about his fellow Oklahoman, the writer Ralph Ellison wrote that it was "when Jimmy's voice began to soar with the spirit of the blues that the dancers – and the musicians – achieve that feeling of communion which was true meaning of the public jazz dance."

Ellison said Rushing began as a singer of ballads, "bringing to them a sincerity and a feeling for dramatizing the lyrics in the musical phrase which charged the banal lines with the mysterious potentiality of meaning which haunts the blues."

[25] According to Gary Giddins, Rushing "brought operatic fervor to the blues,"[26] and of his time with Count Basie notes that "just about every record they made together is a classic.

[30] Rushing was one of eight jazz and blues legends honored in a set of United States Postal Service stamps issued in 1994.