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After high school, Dearie moved to Manhattan to pursue a music career. Dropping her first name, she began to sing in groups such as the Blue Flames (with the Woody Herman Orchestra) and the Blue Reys (with Alvino Rey's band) before starting her solo career.
Dearie moved to Paris in 1952. She formed a vocal group, the Blue Stars (1952–1955), which included Michel Legrand's sister, Christiane, and Bob Dorough. In 1954, the group had a hit in France with a French-language version of "Lullaby of Birdland", arranged by Michel Legrand. The Blue Stars would later evolve into the Swingle Singers. On Dearie's first solo album, released two years later, she played the piano but did not sing.
In 1954, Dearie and King Pleasure recorded "Moody's Mood for Love" (a vocal adaptation by Eddie Jefferson of a James Moody sax solo for "I'm in the Mood for Love") and this is so noted on the Prestige album King Pleasure Sings. One of Dearie's most famous song recordings from that period is "The Riviera", with music by Cy Coleman and lyrics by Joseph McCarthy, in 1956.
After returning from France in 1957, Dearie made her first six American albums as a solo singer and pianist for Verve Records in the late 1950s and early 1960s, mostly in a small trio or quartet setting. Dave Garroway, host of The Today Show and an early fan of Dearie, featured her on several occasions, increasing her exposure with the popular audience. In 1962, Dearie recorded a radio commercial for Hires Root Beer. As it proved very popular, the LP Blossom Dearie Sings Rootin' Songs was released as a premium item that could be ordered for one dollar and a proof of purchase.
In 1964, Dearie recorded the album May I Come In? (Capitol/EMI Records). It was recorded (atypically for her) with an orchestra. During this same period, she performed frequently at New York supper clubs and in 1966 made her first appearance at Ronnie Scott's club in London. Dearie recorded four albums in the United Kingdom during the 1960s that were released on the Fontana label, including a recording of her 1966 performance at Ronnie Scott's. She also performed regularly on Bernard Braden's TV show.
In 1970, after a period of inactivity, Dearie released the album That's Just the Way I Want to Be (including her homage to Dusty Springfield). In 1974, Dearie established her own label, Daffodil Records, which allowed her to have full control of the recording and distribution of her albums. Dearie appeared on television throughout her career, including voice work for the children's educational series Schoolhouse Rock! Some of her pieces in this series were written by her friend Bob Dorough, the jazz singer and composer with whom she performed in Paris in the 1950s. Her voice can be heard on "Mother Necessity", "Figure Eight", and "Unpack Your Adjectives". She received a Grammy nomination in 1973 for Best Recording for Children with the album Multiplication Rock.
The songwriter Johnny Mercer, with whom Dearie collaborated for her 1975 song "I'm Shadowing You", gave one of his final compositions to her for the title song of her 1976 Daffodil album My New Celebrity is You. According to Dearie, she and Mercer were close friends.
In 1983, Dearie was awarded the first Mabel Mercer Foundation Award.
Dearie's voice and songs have been featured on the soundtracks of several films and television shows, including Kissing Jessica Stein, My Life Without Me, The Squid and the Whale, The Adventures of Felix, The Artist, The Marvelous Mrs. Maisel (series), Call the Midwife (series), and Can You Ever Forgive Me?. She also recorded songs with other singers, including Lyle Lovett. She continued to perform in clubs until 2006. She appeared regularly on British television with Peter Cook and Dudley Moore, several times as a guest of Jack Paar on his Tonight show and also appeared on The Danny Kaye Show, The David Frost Show, and The Merv Griffin Show.