Born in Atlanta, Georgia, on July 2, 1920, Windham moved with his partner, Fred Melton, a graphic artist, to New York City in 1939, where he soon became friends with Tennessee Williams, Paul Cadmus, Truman Capote, and Lincoln Kirstein. During World War II, Windham contributed to and edited Kirstein's Dance Index and collaborated with Williams on a stage adaptation of D. H. Lawrence's You Touched Me.

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In 1943, after Melton had married, Windham met Sandy Montgomery Campbell, a Princeton freshman, who became his lifelong partner. An actor and publisher of handsome limited editions, Campbell saw through his press, the Stamperia Valdonega in Verona, many of the first editions of Windham's works until his death in 1988.

Beginning in 1947, Windham began to place short stories in Horizon, The Listener, Botteghe Oscure, and New Directions. He published five novels, one short story collection, and two memoirs. In addition, he contributed essays on artists such as Pavel Tchelitchev, edited Campbell's memoirs, and wrote unpublished stage adaptations of Melville's Billy Budd, Isak Dinesen's The Angelic Avengers, and his own "The Starless Air."

Windham made his major contribution to gay life as a memoirist and editor. In addition to editing his letters from E. M. Forster and Alice B. Toklas, Windham used his diaries to write on Tennessee Williams and Truman Capote. Windham's The Hero Continues, although not intended as a roman à clef, has a protagonist who shares various traits with Williams.

Struck by the inaccuracy of Williams's Memoirs, Windham published Williams's letters to him. However, Williams falsely claimed that Windham had not been granted permission by him and trashed the volume.

Windham's Lost Friendships: A Memoir of Truman Capote, Tennessee Williams, and Others (1987), his best book, not only tells a moving story of the emotional difficulties of two famous writers but also offers insights into the way imagination can be used by artists both to foster their productivity and distort their personal lives. It shows the price demanded by success of two gay men who sought to please a heterosexual public.

In his fiction, Windham treated homosexuality both openly and as a subtext; however, it never becomes his main topic. He published five stories with gay themes: "The Kelly Boys," "The Hitchhiker," "Rome," "The Warm Country," and "Servants with Torches."

The Dog Star (1950), tells of a teenager who, still haunted by the suicide of his best friend, kills himself. The protagonist of The Hero Continues (1960) has a drunken one-night stand with a teen-aged boy. The openly gay-oriented Two People (1965) centers on a married American businessman and the Italian teenager he picks up.

Tanaquil (1972), set in the art world of the 1940s, has as a character a bisexual photographer based on George Platt Lynes. Stone in the Hourglass (1981), a story of art forgery and murder, includes two amusing same-sex bedroom scenes.

Windham died on June 2, 2010 in New York City.

His work remains provocative in its refusal to make simple correlations between same-sex attraction, sexual activity, identity, and self-definition.

Although largely invisible to the general public, a large body of twentieth-century gay male literature by American authors was published prior to Stonewall, some of it positive but most of it tinged with misery or bleakness as the price of being published and disseminated.

Although the question of homosexual identity is a complex one, it has polarized activists, theorists, and literary critics into two primary camps, essentialists and constructionists, both of which can contribute usefully to an understanding of the gay and lesbian literary heritage.

American painter Paul Cadmus is best known for the satiric innocence of his frequently censored paintings of burly men in skin-tight clothes, but he also created works that celebrate same-sex domesticity.

Truman Capote's fiction and autobiographical works helped establish what might be called the quintessential homosexual writing style of the 1950s and 1960s.

One of the finest English novelists of the twentieth century and a tireless defender of humane values, Forster deserves a special place in the gay and lesbian literary heritage.

Although best known for his contributions to the development of American ballet, Lincoln Kirstein was an important figure in the shaping of twentieth-century American culture generally.

For his time, D. H. Lawrence was a maverick in his open and adventurous discussion of all sexual issues and especially homosexuality, both male and female.

American photographer George Platt Lynes made his fame as a fashion and portrait photographer, but his greatest work may have been his dance images and male nudes.

The most important American novelist of the nineteenth century, Herman Melville reflects his homosexuality throughout his texts.

Russian-born painter, sculptor, and set designer Pavel Tchelitchew created a number of works that illustrate homoerotic desire.

Conflicted over his own sexuality, Tennessee Williams wrote directly about homosexuality only in his short stories, his poetry, and his late plays.