Dinah Washington was born Ruth Lee Jones on August 29, 1924, in Tuscaloosa, Alabama, and was taken to Chicago as a small child; the Encyclopedia of Alabama puts the move at around her fourth year. Church music shaped her first: she played piano for the choir at St. Luke's Baptist Church while still in elementary school, directed a church choir in her teens, and sang with the Sallie Martin Gospel Singers. After winning an amateur contest at the Regal Theater at fifteen she moved into nightclub work, and by 1941-42 she was singing at Chicago rooms including Dave's Café and the Downbeat Room of the Sherman Hotel, where she shared a bill with Fats Waller. A friend took her to hear Billie Holiday at the Garrick Stage Bar, and the club's owner, Joe Sherman, was so taken with her version of "I Understand" that he hired her for the room upstairs. She picked up the name Dinah Washington during that engagement, though accounts differ on who suggested it: Sherman, the agent Joe Glaser, and Lionel Hampton himself have each been credited.

Hampton came to hear her at the Garrick and offered her a place as the female vocalist of his orchestra, and she sang with the band from 1943 to 1946. Her first records were made for Keynote in New York on December 29, 1943, a blues session organized by the critic Leonard Feather with a sextet drawn from Hampton's band, including trumpeter Joe Morris, tenor saxophonist Arnett Cobb and pianist Milt Buckner. "Evil Gal Blues," written by Feather, and its follow-up "Salty Papa Blues" both reached Billboard's Harlem Hit Parade. In December 1945, in Los Angeles, she recorded a set of blues sides for the Apollo label with a group led by tenor saxophonist Lucky Thompson that also included vibraphonist Milt Jackson and bassist Charles Mingus.

She left Hampton in 1946 and signed with Mercury as a solo artist; her first Mercury record was a version of Fats Waller's "Ain't Misbehavin'." Between 1948 and 1955 she placed 27 records in the R&B top ten. "Am I Asking Too Much" (1948) and "Baby Get Lost" (1949) both reached number one on the R&B chart, "I Wanna Be Loved" (1950) crossed over to number 22 on the pop chart, and "Teach Me Tonight" (1954) later entered the Grammy Hall of Fame. Alongside the hits she kept recording with jazz players. On August 14, 1954, in Los Angeles, she sang before a studio audience with the newly formed Clifford Brown-Max Roach quintet, joined by trumpeters Clark Terry and Maynard Ferguson, altoist Herb Geller and tenor saxophonist Harold Land. The results came out in early 1955 as Dinah Jams on EmArcy, Mercury's jazz imprint, and a companion instrumental album from the same session, Jam Session, includes her on one track.

EmArcy followed with a run of jazz-oriented albums. After Hours with Miss D (1954) paired her with Clark Terry and tenor saxophonist Eddie "Lockjaw" Davis, and For Those in Love, recorded in March 1955 with arrangements by Quincy Jones, used an eight-piece band that included Wynton Kelly and Jimmy Cobb; Dan Morgenstern's liner notes compared her to Billie Holiday. In the Land of Hi-Fi (1956) featured Cannonball Adderley, and The Swingin' Miss "D" (1957) put her in front of a Quincy Jones orchestra recorded over several days in December 1956. Songbook albums devoted to Fats Waller (with her then husband, tenor saxophonist Eddie Chamblee, as duet partner) and Bessie Smith (1958) followed. She appeared at the Newport Jazz Festival every year from 1955 through 1959, and her July 6, 1958 set, with arrangements by trombonist Melba Liston and a band that included Max Roach, vibraphonist Terry Gibbs and Wynton Kelly, was issued as Newport '58; she is also heard singing "All of Me" in the film Jazz on a Summer's Day. She was a regular at Birdland in 1958 and in 1961-62, performed with Count Basie and Duke Ellington in 1963, and in 1960 Leonard Feather included her among the "Giants of Jazz" in his Encyclopedia of Jazz.

In 1959 she had her first top-ten pop hit with "What a Diff'rence a Day Makes," from the album What a Diff'rence a Day Makes!, arranged and conducted by Belford Hendricks with a rhythm section of Kenny Burrell, Joe Zawinul, bassist Milt Hinton and drummer Panama Francis; the single reached number 4 on the pop chart and won the Grammy Award for Best Rhythm & Blues Performance at the second annual Grammy Awards. "Unforgettable" followed, then two duets with Brook Benton in 1960, "Baby (You've Got What It Takes)" and "A Rockin' Good Way (to Mess Around and Fall in Love)," both number one on the R&B chart. Her last big hit was "September in the Rain" (1961). In 1962 she moved to Roulette, where Henry Glover produced much of her remaining output, among it Back to the Blues (1963) and We Three (1963), a shared-billing LP with Sarah Vaughan and Joe Williams.

Washington died in Detroit on December 14, 1963, at the age of 39. Her husband at the time, the football player Dick "Night Train" Lane, found her unresponsive; an autopsy attributed the death to a combination of the sedatives secobarbital and amobarbital, prescribed for insomnia and dieting, and it was ruled accidental. She is buried at Burr Oak Cemetery in Alsip, Illinois. The number of her marriages is uncertain, with sources giving anywhere from six to nine. She was inducted into the Big Band and Jazz Hall of Fame in 1984, the Alabama Jazz Hall of Fame in 1986 and the Rock and Roll Hall of Fame in 1993, and three of her recordings, "What a Diff'rence a Day Makes," "Teach Me Tonight" and "Unforgettable," are in the Grammy Hall of Fame. Aretha Franklin recorded the tribute album Unforgettable: A Tribute to Dinah Washington in 1964.

Washington was billed as the Queen of the Blues, a title she herself attributed to Bessie Smith, and her catalog crosses blues, rhythm and blues, traditional pop and jazz, which is why writers disagree about how far to call her a jazz singer: one jazz reference notes she was never strictly one, while her Wikipedia entry calls her primarily a jazz vocalist, and her EmArcy sessions, her Hampton years and her place in the jazz halls of fame make the jazz case. The AllMusic biographer Richard S. Ginell described a gritty, high-pitched voice with absolute clarity of diction and clipped, bluesy phrasing, and noted that critics who accused her of trading art for commerce were reacting to the same adaptability that her fans loved. Quincy Jones said she could take a melody apart and rebuild it while every syllable stayed clear. Her sources were gospel, Bessie Smith's blues repertoire and the example of Billie Holiday, whom she heard at the Garrick as a teenager; her influence runs through the soul and pop singers who followed, most visibly Aretha Franklin in her 1964 tribute album, and Tony Bennett has recalled that performers from the other Las Vegas Strip shows would come out the night she was in town. Her jazz recordings are at their strongest when a small band leaves her room to phrase freely, as on Dinah Jams and For Those in Love, while the later Mercury and Roulette albums lean toward string and chorus arrangements that critics have long argued over.