Ciardi was born at home in Boston's Little Italy. After the death of his father in 1919, he was raised by his Italian mother (who was illiterate) and his three older sisters, all of whom scrimped and saved until they had enough money to send him to college. "In 1921, two years after his father was killed in an automobile accident, the family moved to Medford, Massachusetts, where the young Ciardi peddled vegetables to the neighbors and attended public schools." "Ciardi began his higher studies at Bates College in Lewiston, Maine, but transferred to Tufts University in Boston, where he studied under the poet John Holmes." "He received his degree in 1938, and won a scholarship to the University of Michigan, where he obtained his master's degree the next year and won the first of many awards for his poetry," i.e., the prestigious Hopwood Award in poetry.

Ciardi taught briefly at the University of Kansas City before joining the United States Army Air Corps in 1942, becoming a gunner on B-29 and flying some twenty missions over Japan before being transferred to desk duty in 1945. He was discharged in October 1945 with the rank of Technical Sergeant and with both the Air Medal and Oak Leaf Cluster. Ciardi's war diary, Saipan, was published posthumously in 1988. After the war, Ciardi returned to UKC for the spring semester 1946, where he met and married Myra Judith Hostetter on July 28 (who at the time was a journalist and journalism instructor). Immediately after the wedding, the couple left for a third-floor apartment at Ciardi's Medford, Massachusetts home, which his mother and sisters had put together for the man of their family and his new bride.

John Ciardi was a longtime resident of Metuchen, New Jersey. He died on Easter Sunday in 1986 of a heart attack, but not before composing his own epitaph:

Here, time concurring (and it does);Lies Ciardi. If no kingdom come,A kingdom was. Such as it wasThis one beside it is a slum.

"After the war, Mr. Ciardi returned briefly to Kansas State, before being named instructor [in 1946], and later assistant professor, in the Briggs Copeland chair at Harvard University, where he stayed until 1953." "While at Harvard, Mr. Ciardi began his long association with the Bread Loaf Writers Conference at Middlebury College in Vermont, where he lectured on poetry for almost 30 years, half that time as director of the program."

Ciardi had published his first book of poems, Homeward to America, in 1940, before the war, and his next book, Other Skies, focusing on his wartime experiences, was published in 1947. His third book, Live Another Day, came out in 1949. In 1950, Ciardi edited a poetry collection, Mid-Century American Poets, which identified the best poets of the generation that had come into its own in the 1940s: Richard Wilbur, Muriel Rukeyser, John Frederick Nims, Karl Shapiro, Elizabeth Bishop, Theodore Roethke, Delmore Schwartz, Randall Jarrell, Robert Lowell, Ciardi himself, and several others. Each poet selected several poems for inclusion, plus his or her comments on the poetic principles that guided the compositions, addressing especially the issue of the so-called "unintelligibility" of modern poetry.

Ciardi had begun translating Dante for his classes at Harvard and continued with the work throughout his time there. His translation of The Inferno was published in 1954. Dudley Fitts, himself an important mid-century translator, said of Ciardi's version, "[H]ere is our Dante, Dante for the first time translated into virile, tense American verse; a work of enormous erudition which (like its original) never forgets to be poetry; a shining event in a bad age." Joan Ross Acocella, however, noted “The constant stretching for a heartier, more modern and American idiom not only vulgarizes; it also guarantees that wherever Dante expresses himself by implication rather than by direct statement, Ciardi will either miss or ignore the nuance.” The translation "is widely used at universities." Ciardi's translation of The Purgatorio followed in 1961 and The Paradiso in 1970. Ciardi's version of Inferno was recorded and released by Folkways Records in 1954. Two years later, Ciardi would have his work featured again on an album entitled, As If: Poems, New and Selected, by John Ciardi.

In 1953, Ciardi joined the English Department at Rutgers University in order to begin a writing program, but after eight successful years there, he resigned his professorship in 1961 in favor of several other more lucrative careers, especially fall and spring tours on the college lecture circuit, and to "devote himself fulltime to literary pursuits." (When he left Rutgers, he famously quipped that teaching was "planned poverty.") He was popular enough and interesting enough to warrant a pair of appearances in the early 1960s with Johnny Carson on The Tonight Show. "Poetry editor of Saturday Review from 1956 to 1972, he wrote the 1959 poetry textbook How Does A Poem Mean." Ciardi was a "fellow of the National Academy of Arts and Sciences and a member and former president of the National Institute of Arts and Letters." From 1980 until his death, "he produced a weekly three-minute spot on etymology, or the study of the origin of words, for National Public Radio entitled Word In Your Ear." He also taught at the University of Florida.

For the last decade of his life, he reported on word histories on National Public Radio's Morning Edition, as an outgrowth of his series of books of etymologies, A Browser's Dictionary (1980), A Second Browser's Dictionary (1983) and Good Words to You (posthumously published in 1987). Among 20th-century American men of letters, he maintained a notably high profile and level of popularity with the general public, as well as a reputation for considerable craftsmanship in his output. Burton Raffel summed up Ciardi's career as follows: “Blessed with a fine voice, a ready wit, and a relentless honesty, Ciardi became in many ways an archetype of the existentially successful twentieth-century American poet, peripatetic, able to fit into and exploit chinks in the great American scheme of things, while never fitting in as either a recognized peg or hole.”

Critic and poet Kenneth Rexroth described Ciardi as ". . . singularly unlike most American poets with their narrow lives and feuds. He is more like a very literate, gently appetitive, Italo-American airplane pilot, fond of deep simple things like his wife and kids, his friends and students, Dante's verse and good food and wine." "During his years at Bread Loaf and at the Saturday Review, Ciardi established a reputation as a tough, sometimes harsh, critic." "His review of Anne Morrow Lindbergh's 1956 book The Unicorn touched off what the Review's editor, Norman Cousins, described as the biggest storm of reader protest in the magazine's history." "Ciardi defended his stand, noting that it was the reviewer's duty to damn when warranted." May Sarton, for example, accused Ciardi of "hat[ing her] guts and [of doing] everything he could to destroy [her]" in describing the difficulties faced by women poets.

Ciardi did not fare well during the counterculture of the late 1960s and 1970s. He had been a fresh, sometimes brash, voice for modern poetry, but as he approached his fiftieth birthday in 1966, he had become entrenched and his voice became bitter, sometimes bumptious. He urged his only remaining students, those at Bread Loaf for two weeks each August, to learn how to write within the tradition before abandoning it in favor of undisciplined, improvisational free verse. Ciardi was unceremoniously fired from Bread Loaf in 1972, after serving seventeen years as director, and not having missed a single year on the poetry staff since 1947.

Over the past quarter century, John Ciardi has come to be regarded as a mid-level, mid-century formalist, one who was replaced in literary history by the more daring and colorful Beat, Confessional, and Black Mountain poets. However, with revisionism chipping away at the reputations of the latter groups, and the emergence of Dana Gioia and the New Formalists in the late twentieth century, Ciardi's type of mostly understated verse, what he praised as the Unimportant Poem, reads much better than it has in many years. His best poems in collections like his verse autobiography, Lives of X (1971) or the opening sequence of bird poems in Person to Person (1964), or several of his love poems in I Marry You (1958) or the many Italian American poems that are sprinkled throughout his Collected Poems (1997)--all have a quietly assertive voice that pleases.

In recognition of Ciardi's work, a John Ciardi Lifetime Achievement Award for Poetry given annually to an Italian American poet for lifetime achievement in poetry.

National Public Radio (NPR) continues to make Ciardi's commentaries available. Etymologies and commentary on words such as daisy, demijohn, jimmies, gerrymander, glitch, snafu, cretin, and baseball, among others, are available from the archives of NPR's website.

NPR also began making his commentaries available as podcasts, starting in November 2005.

"In 1956, Ciardi received the Prix de Rome from the American Academy of Arts and Letters. In 1982, the National Council of Teachers of English awarded him its award for excellence in children's poetry." He also won American Platform Association's Carl Sandburg Award in 1980.