James Lapine was born in Mansfield, Ohio and lived there until his early teens when his family moved to Stamford, Connecticut. He attended public schools before entering Franklin and Marshall College in Lancaster, Pennsylvania where he majored in History. He went on to get an MFA in Design from the California Institute of the Arts in Valencia.

After graduate school, he moved to New York City where he worked part-time as a waiter; a page and tour guide at NBC; a free-lance photographer and graphic designer; and an architectural preservationist for the Architectural League of NY. One of his free-lance jobs was designing the magazine of the Yale School of Drama, yale/theatre. The dean of the School of Drama, Robert Brustein subsequently offered Lapine a full-time job designing all of the printed materials for the School of Drama and the Yale Repertory Theatre as well as a faculty position teaching a course in advertising design.

While at Yale, his students urged him to direct a play during the annual January period when both faculty and students undertook a project outside of their areas of study or expertise. At their suggestion Lapine directed a Gertrude Stein piece, Photograph. The play was five acts, and just three pages in length. Assembling students and friends, it was presented in New Haven and came to the attention of director Lee Breuer who helped arrange for a small performance space in Soho to produce the work for three weeks. The production was enthusiastically received by The New York Times and won Lapine an Obie award. Lapine was then approached to create a new piece for the Music Theatre Group. He wrote and directed a workshop version of Twelve Dreams, a work inspired by a Jungian case history. The play was later presented at the Public Theater and revived by Lincoln Center Theater.

Lapine eventually left the visual arts for a career in the theatre where he has also written and directed the plays Table Settings; Luck, Pluck and Virtue; The Moment When; Fran's Bed and Mrs. Miller Does Her Thing. Among his many other off-Broadway offerings were three Shakespeare productions for the Public Theatre.

On Broadway he has written the book for and directed Stephen Sondheim’s Sunday in the Park with George; Into the Woods; Passion; and the multi-media revue Sondheim on Sondheim. He also directed Merrily We Roll Along as part of Encores at New York City Center. With William Finn he has collaborated on March of the Falsettos and Falsettoland, later presented on twice Broadway as Falsettos; A New Brain; Muscle; and Little Miss Sunshine. He has also directed on Broadway David Henry Hwang’s Golden Child; The Diary of Anne Frank; Michel Legrand’s Amour; The 25th Annual Putnam County Spelling Bee; the 2012 revival of Annie, and his stage adaptation of the famous Moss Hart autobiography Act One, which premiered at Lincoln Center Theater on the Beaumont stage.

With Frank Rich he co-produced and also directed the HBO documentary Six by Sondheim for which he received an Emmy nomination and a Peabody award. Lapine wrote the screenplay for the film version of Into the Woods directed by Rob Marshall and the film Custody which he also directed.

His book, Putting it Together: How Stephen Sondheim and I Created Sunday in the Park with George was released in August 2021 and immediately made it to the New York Times bestseller list. He is also completing a documentary In the Company of Rose about the life and times of Rose Styron: the poet, human rights activist and widow of the famed author William Styron. His collaboration with composer Tom Kitt and lyricist Michael Korie, Flying Over Sunset, will premiere December 13th on Broadway for Lincoln Center Theater. He has written the book and directed, collaborating with the celebrated contemporary choreographer Michelle Dorrance.

Lapine has been nominated for twelve Tony Awards winning on three occasions and has received five Drama Desk Awards and the Pulitzer Prize. In 2011, he was inducted into the Theater Hall of Fame and in 2015 was the recipient of the Mr. Abbott Award presented by the Society of Stage Directors and Choreographers for a lifetime of exceptional achievement in the theatre. Lapine is a member of the Dramatist Guild Council and for the last twenty years has been a mentor for TDF's Wendy Wasserstein Project which introduces the world of theater to a select group of underserved students from New York City public high schools.