Cunningham was born in Cincinnati, Ohio, and grew up in Pasadena, California. He studied English literature at Stanford University where he earned his degree. Later at the University of Iowa he received a Michener Fellowship and was awarded a Master of Fine Arts degree from the Iowa Writers' Workshop. While studying at Iowa, he had short stories published in the Atlantic Monthly and the Paris Review. His story "White Angel," from his novel A Home at the End of the World was included in "The Best American Short Stories, 1989," published by Houghton Mifflin.

In 1993 he received a Guggenheim Fellowship and in 1998 a National Endowment for the Arts Fellowship. In 1995 he was awarded the Whiting Writers' Award. Cunningham has taught at the Fine Arts Work Center inProvincetown, Massachusetts and in the creative writing MFA program at Brooklyn College. He is currently professor of creative writing at Yale University.

Although Cunningham is gay and has been in a monogamous partner for 18 years with psychoanalyst and artist Ken Corbett, he dislikes being referred to as only a "gay writer", according to a PlanetOut article PlanetOut Entertainment because while being gay does greatly influence his work, he feels that it is not (and should not be) his defining characteristic.

The Hours established Cunningham as a major force in American writing, and his most recent novel, Specimen Days, was also well received by American critics. Cunningham has edited a book of poetry and prose by Walt Whitman, Laws for Creations, and has co-written, with Susan Minot, a screenplay adapted from Minot's novel Evening. He is also a producer for the 2007 film, Evening, which stars Glenn Close, Toni Collette, and Meryl Streep.

Novels

• 1984 Golden States
• 1990 A Home at the End of the World
• 1995 Flesh and Blood
• 1998 The Hours
• 2005 Specimen Days
• 2010 By Nightfall

Nonfiction

• 2002 Lands End: A Walk in Provincetown

Screenplays

• 2004 A Home at the End of the World
• 2007 Evening

Contributor

• 2000 Drawn By The Sea (exhibition catalogue text; 110 signed copies)
• 2001 The Voyage Out by Virginia Woolf (Modern Library Classics edition) (Introduction)
• 2001 I Am Not This Body: The Pinhole Photographs of Barbara Ess (Text)
• 2004 Washington Square by Henry James (Signet Classics edition) (Afterword)
• 2004 Death In Venice by Thomas Mann (new translation by Michael Henry Heim) (Introduction)
• 2006 Laws for Creations, Poems by Walt Whitman (Editor and introduction)
• 2007 a Memory, a Monologue, a Rant, and a Prayer edited by Eve Ensler and Mollie Doyle (Short Story, The Destruction Artist)

• "White Angel" was included in the 1989 Best American Short Stories.
• "Mr. Brother" was included in the 1999 O. Henry Prize Stories.

For The Hours, Cunningham was awarded the:

• Pulitzer Prize for Fiction - 1999
• PEN/Faulkner Award - 1999
• Gay, Lesbian, Bisexual, and Transgendered Book Award - 1999