Berryman graduated from Columbia University in 1936. A pamphlet entitled Poems was published in 1942 and his first proper book, The Dispossessed, appeared six years later. Of his youthful self he said, 'I didn't want to be like Yeats; I wanted to be Yeats.' His first major work, in which he began to develop his own unique style of writing, was Homage to Mistress Bradstreet, which appeared in Partisan Review in 1953 and was published as a book in 1956. Another pamphlet, His thought made pockets & the plane buckt, followed. It was the collection called Dream Songs that earned him the most admiration. The first volume, entitled 77 Dream Songs, was published in 1964 and won the Pulitzer Prize for poetry. The second volume, entitled His Toy, His Dream, His Rest, appeared in 1968. The two volumes were combined as The Dream Songs in 1969. By that time Berryman, though not a "popular" poet, was well established as an important force in the literary world, and he was widely read among his contemporaries. In 1970 he published the drastically different Love & Fame. It received many negative reviews, along with a little praise, most notably from Saul Bellow and John Bailey. Despite its negative reception, its colloquial style and sexual forthrightness have influenced many younger poets, especially from Britain and Ireland. Delusions Etc., his bleak final collection, which he prepared for printing but did not live to see appear, continues in a similar vein. Another book of poems, Henry's Fate, culled from Berryman's manuscripts, appeared posthumously, as did a book of essays, The Freedom of the Poet, and some drafts of a novel, Recovery.

The poems that form Dream Songs involve a character who is by turns the narrator and the person addressed by a narrator. Because readers assumed that these voices were the poet speaking directly of himself, Berryman's poetry was considered part of the Confessional poetry movement. Berryman, however, scorned the idea that he was a Confessional poet.

While Berryman was on the faculty of the University of Iowa Writers' Workshop, W. D. Snodgrass, the original confessional poet, was one of the members of his class. "I have been very fortunate twice in my career as a student of poetry," William Dickey wrote in Ed Dinger's Seems Like Old Times, "first to have been at Reed College as an undergraduate with Gary Snyder, Philip Whalen and Lew Welch, second to have been in John Berryman's extraordinary and intense poetry workshop with W. D. Snodgrass, Donald Justice, Philip Levine, Paul Petrie, Robert Dana, Constance Urdang, Jane Cooper, Donald Finkel, Henri Coulette...the list continues beyond the capacity of my memory, but it was a course I approached with rapture and fear, owing in part to Berryman's sometimes jagged abruptness, as when, having warned me beforehand that he was going to exhibit the profound mortality of one of my works, he held it out at arm's length in the class, looked at it with loathing, and said, 'Now, what are we to say about this ridiculous poem?'"

"I remember a day in the old tin barracks that served as our classroom down by the river, when John Berryman scribbled some lines of mine on the blackboard," Robert Dana added. "'Dana!' he shouted across two rows of chairs, 'Do you know what that is?' He rapidly marked the scansion. 'Metrical chaos! that's what that is! Metrical chaos!'" But chaos was a large and natural part of Berryman's own life, including his poetry:

"It was that kind of blow-torch approach that cut Berryman's class, in two weeks, from about 40 to thirteen." Dana continued. "I like to think of us now as 'The Lucky Thirteen,' but we were crazy too. Crazy with the kind of toughness it took to hang in there against John's special mix of crankiness, brilliance, and cruelty. And we were brash in our own ways.

"Phil Levine punched Berryman in the eye one night, breaking a pair of glasses and establishing a life-long friendship." These kinds of personal relationships were always of great importance to Berryman. It is a question whether he influenced his students more than they influenced him.

On the other hand, the UK poet and contemporary of W. H. Auden, Stephen Spender, did not believe that this sort of hot-house atmosphere was necessarily good for poets. Spender has written, "The bad...or perhaps I should say the tragic...result of campus patronage [in the U.S.] is the depressing effect it sometimes has on major talents. I think that the tragic and near-suicidal deaths of Randall Jarrell, Theodore Roethke and John Berryman are not unconnected with their being in positions where, although they were admired, they were very isolated."

In 1926, when the poet was twelve, his father, John Allyn Smith, Sr., a banker in Minneapolis, shot himself. After his father's death, the poet's mother remarried, and thus he came to his new surname of Berryman. The vision of his father's suicide haunted John Berryman's poetic imagination, and the subject is addressed indirectly in the Dream Songs several times and directly once, where the poet wishes that he could kill the corpse of his father. Berryman was an alcoholic, and friends reported that even as a student at Columbia University he was two different people when drinking and sober. As a mature poet, Berryman's alcoholism and depression interfered with his ability to give readings, to speak in public, and to work appropriately. On the morning of January 7, 1972, Berryman killed himself by jumping from the Washington Avenue Bridge in Minneapolis, Minnesota.

The Dream Songs are eighteen-line poems in three stanzas. Each individual poem is lyric and organized around an emotion provoked by an everyday event. The tone of the poems is less surreal than associational or intoxicated.The principal character of the song cycle is Henry, who is both the narrator of the poems and referred to by the narrator in the poems.

In 1967 Berryman published a book of near-juvenilia, Berryman's Sonnets, of which the author wrote in a verse preface, speaking of himself in the third person, "He made, a thousand years ago, a-many songs / for an Excellent Lady, wif whom he was in wuv, / shall he now publish them?" Perhaps he should. "So free them to the winds that play, / let boys & girls with these old songs have holiday / if they feel like it (ix)."

Berryman's archness notwithstanding, the collection was interesting because it shows that his distinctive poetic diction had roots well back in his creative life. Thus Sonnet 102:

A penny, pity, for the runaway ass!

A nickel for the killer's twenty-six-mile ride!

Ice for the root rut-smouldering inside!

Eight hundred weeks I have not run to Mass....

Toss Jack a jawful of good August grass!

'Soul awful,' pray for a soul sometimes has cried!

Wire reasons he seasons should still abide!

Hide all your arms where he is bound to pass....

Who drew me first aside? her I forgive,

Or him, as I would be forgotten by

O be forgiven for salt bites I took.

Who drew me off last, willy-nilly, live

On (darling) free. If we meet, know me by

Your own exempt (I pray) and earthly look.

In Berryman's early pieces the neo-Elizabethan imagination and metaphysical wit of Homage to Mistress Bradstreet and his other books, with the posthumous Delusions, Etc., which was published in 1972, are linked with the passion of youth, causing some readers to wish that the later Berryman had retained some of the charm and commitment to blood found in the Sonnets, instead of going far down the road toward arch confession and idiosyncratic style, as he did in his later work.

The poet and critic Robert Phillips wrote that the poet's second collection "is filled with accounts of friends' deaths and suicides, events which took their toll on Berryman's psyche: Randall Jarrell, Theodore Roethke, Sylvia Plath, R. P. Blackmur, Yvor Winters, William Carlos Williams, and above all, Delmore Schwartz, to whose memory Berryman dedicated the book and penned Dream Songs 146—157 and also number 344. These personal losses were experienced during a time of great public loss as well: John Kennedy, Robert Kennedy, Martin Luther King, Ernest Hemingway, William Faulkner. Yet none of these personal or public deaths figure so importantly in the volume as the suicide of Berryman's father which is, in one sense, the sole subject of the latter collection (93)." Berryman's own suicide was not the first among the Confessional poets.

As he developed the Dream Songs, Berryman got more elaborate and obscure. "Berryman is a poet so preoccupied with poetic effects as to be totally in their thrall," James Dickey wrote. "His inversions, his personal and often irritatingly cute colloquialisms and deliberate misspellings, his odd references, his basing of lines and whole poems on private allusions, create what must surely be the densest verbal thickets since Empson's."

In his 366th "Dream Song" Berryman himself wrote, "These Songs are not meant to be understood, you understand. / They are only meant to terrify & comfort." "And understood many have not been," Phillips wrote. "Packed with private jokes, topical and literary allusions (Berryman's reading and personal library are legendary), they boggle many minds. When the first 77 Dream Songs...were published, Robert Lowell admitted, 'At first the brain aches and freezes at so much darkness, disorder and oddness. After a while, the repeated situations and their racy jabber become more and more enjoyable, although even now I wouldn't trust myself to paraphrase accurately at least half the sections.'" Phillips continued, "The situation was considerably beclouded when four years later, Berryman dumped on the world a truckful of 308 additional Dream Songs, under the title His Toy, His Dream, His Rest."

Though his work was experimental, Berryman still remained a formalist at heart, inventing not only a poetic diction and a style of writing that is clearly recognizable as his own but a specific poem-form as well as exhibited in his Dream Songs. The Dream Song form consists of three stanzas with six lines per stanza. Each stanza also contained its own (often irregular) rhyme scheme.

Another distinctive feature of the poems had to do with their narrative voices. These were not, strictly speaking, first-person confessional poems, for they often contained multiple voices in dialogue, including "Henry," an unnamed character who refers to Henry as "Mr. Bones," and an "I," which may be read as the voice of the poet himself.

There was, then, a distinct dramatic element in the Dream Songs, as in no. 80, "Op. posth. no. 3," from His Toy, His Dream, His Rest:

It's buried at a distance, on my insistence, buried.

Weather's severe there, which it will not mind.

I miss it.

O happies before & during & between the times it got

:married

I hate the love of leaving it behind,

deteriorating & hopeless that.

The great Uh climbed above me, far above me,

doing the north face, or behind it. Does He love me?

over, & flout.

Goodness is bits of outer God. The house-guest

(slimmed down) with one eye open & one breast

:out.

Slimmed-down from by-blow; adoptive-up; was white.

A daughter of a friend. His soul is a sight.

Mr Bones, what's all about?

Girl have a little: what be wrong with that?

You free?...Down some many did descend

from the abominable & semi-mortal Cat.

This is one of the few poems in The Dream Songs that has a title, and from it the reader can infer a subject: the speaker's death. Since the speaker of the poem is dead and the poem itself is not only published, but composed, after the speaker's demise, then one may also infer that it is a dramatic poem, the speaker imagining himself both as dead and alive and writing what amounts to an elegy for himself. The "it" of the first three lines is the speaker's corpse, which the "I" misses. "It" was happy at times in its life. The "I" must leave "it" behind...an odd twist, since usually it is the person dying who leaves the living "behind." The "I" will probably be assumed by most readers to be the soul of the "it."

Where is the "I" going, then? He has followed "the great Uh" which "climbed above" the "I," upon the "north face"...this is mountaineering talk. "Uh" has climbed beyond "I." Does "Uh" love "I"? "over, & flout." What is over? Who is flouting whom?

"The house-guest" is obscure until one recalls that the coffin has in English literary traditions been called "the narrow house." The "it" is "slimmed down" to a skeleton "with one eye open" and its "breast out."

The third stanza explains that before "it" was buried "it" began to be "slimmed down" before death as a result of a "by-blow," another seemingly obscure word which is cleared up by reference to the O.E.D.: The third definition of "by-blow" is "One who comes into the world by a side-stroke; an illegitimate child, a bastard." The rest of the line thus clears up: "adoptive-up; was white." The next line is a bit cloudier, "A daughter of a friend. His soul is a sight." But we can be a bit easier in our assumption that "I" is the soul of "it."

Who is the speaker? In a preface to The Dream Songs, Berryman wrote, "The poem ... is essentially about an imaginary character (not the poet, not me) named Henry, in early middle age ... who ... talks about himself sometimes in the first person, sometimes in the third, sometimes even in the second; he has a friend, never named, who address him as Mr Bones and variants thereof." It becomes obvious through his description that "Henry" and "Mr Bones" are one and the same, and that Henry is the primary speaker. A change in speaker, to the unnamed friend who addresses Henry as Mr Bones (or back to Henry), is signified by a dash, as in the last 2 lines of his fourth "Dream Song:" "There ought to be a law against Henry / -Mr. Bones: there is."

It has been presumed that both "Henry" and "Mr Bones" are aspects of Berryman himself; if Mr. Bones is not, then perhaps...some critics say, taking their cue from the word "bones" -- he is Death who stalks the poet, although Berryman's statements refute that Mr Bones is actually a separate character. One can maintain with good circumstantial backing, however, that Henry is at least "Mr. Interloc'tor," the master of ceremonies of the traditional minstrel show that is Berryman's life, and that the character who refers to Henry as Mr Bones is the blackface end-man who is the thorn in the side of the emcee. Berryman has said that "Henry" was his dentist. On other occasions, he suggested that the choice of name originated from a conversation with his wife, where they agreed on the worst male and female names ever, "Henry" and "Mabel," and grew to affectionately call each other these names.

Okkervil River's song "John Allyn Smith Sails" from their 2007 album The Stage Names is about John Berryman.

The Hold Steady's song "Stuck Between Stations" from the album Boys and Girls in America relates a loose rendition of Berryman's death, describing the isolation he felt, despite his critical acclaim, and depicting him walking with the Devil on the Washington Avenue Bridge, ending with "We all come down and drown in the Mississippi River." (The lyricist, Craig Finn, is a native of Minneapolis.)The lyric is:

The Devil and John Berryman took a walk togetherThey ended up on Washington talking to the riverHe said "I surrounded myself with doctors and deep thinkersBut big heads with soft bodies make for lousy lovers".There was that night that we thought that John Berryman could fly.But he didn't so he died.She said "you're pretty good with words but words won't save your life"And they didn't so he died.He was drunk and exhausted, but he was critically acclaimed and respected.

"Mama, Won't You Keep Those Castles in the Air and Burning?", a song from Clap Your Hands Say Yeah's album Some Loud Thunder references John Berryman.

The song "We Call Upon the Author" from the 2008 Nick Cave and the Bad Seeds album Dig, Lazarus, Dig!!! contains the lyric "Bukowski was a jerk! Berryman was best!", and goes on to compare his poetry to "wet papier-mâché", adding that "he went the Hemingway"...a reference to the fact that both writers committed suicide..."Weirdly on wings, and with maximum pain."