Foote began as an actor after studying at the Pasadena Playhouse in 1931–32. After getting better reviews for plays he had written than his acting, he focused on writing in the 1940s and became one of the leading writers for television during the 1950s, beginning with an episode of The Gabby Hayes Show. The Trip to Bountiful premiered March 1, 1953 on NBC with the leading cast members (Lillian Gish, Eva Marie Saint) reprising their roles on Broadway later that year. Throughout the 1950s, Foote wrote for The Gulf Playhouse, The Philco Television Playhouse, The United States Steel Hour, Playwrights ’56, Studio One, Armchair Theatre and Playhouse 90. He continued into the 1960s with ITV Playhouse and DuPont Show of the Month. He adapted William Faulkner’s “Old Man” to television twice, in 1959 and 1997; receiving Emmy nominations both years and winning for the 1997 drama (Outstanding Writing of a Miniseries or Special).

Foote’s plays were produced on Broadway, Off-Broadway, Off-Off-Broadway and at many regional theatres. He wrote the English adaptation of the original Japanese book for the 1970 musical Scarlett, a musical adaptation of Gone with the Wind. He won the 1995 Pulitzer Prize for Drama for The Young Man From Atlanta. The Goodman Theatre production that was presented on Broadway in New York City in 1997 was nominated for Best Play, but did not win. The production starred Rip Torn, Shirley Knight and Biff McGuire. Knight and McGuire were also nominated for Tony Awards.  In 1996, Foote was inducted into the American Theater Hall of Fame.

In 2000, Foote was honored with the PEN/Laura Pels International Foundation for Theater Award as a Master American Dramatist.  His nine-play biographical series, mainly about his father, The Orphans’ Home Cycle (Roots in a Parched Ground, Convicts, Lily Dale, The Widow Claire, Courtship, Valentine’s Day, 1918, Cousins, and The Death of Papa) ran in repertory off-Broadway in 2009–2010. The combined productions received a Special Drama Desk Award “To the cast, creative team and producers of Horton Foote’s epic The Orphans’ Home Cycle”. Parts of the series had been produced as separate plays previously; Convicts, Lily Dale, Courtship, Valentine’s Day and 1918 were filmed, the latter three being shown on PBS as a mini-series titled The Story of A Marriage.  Foote received an Academy Award for Writing Adapted Screenplay and the Writers Guild of America Screen Award for his adaptation of To Kill a Mockingbird in 1962. Foote did not attend the Oscars ceremony because he did not expect to win, and so was not present to collect the award in person.  Foote personally recommended actor Robert Duvall for the part of Boo Radley in To Kill a Mockingbird after meeting him during a 1957 production of The Midnight Caller at Neighborhood Playhouse in New York City. The two would work together many more times in the future. Foote has described Duvall as “our number one actor”.

Foote’s script for the 1983 film Tender Mercies had been rejected by many American film directors before Australian director Bruce Beresford finally accepted it; Foote later said, “this film was turned down by every American director on the face of the globe.” Foote was rumored to have written the lead role of Tender Mercies specifically for Robert Duvall. Foote denied this, claiming it would be too constraining for him to write a role for a specific actor; however, Duvall said he helped contribute some ideas for the character, and said Foote knew he had wanted to play a country western singer. The film received six Academy Awards nominations, including Best Picture (which lost) and Best Original Screenplay (which Foote won). Duvall also won an Academy Award for his performance. Well aware of his failure to attend the 1963 ceremony, Foote made sure to attend the 1984 ceremony. The film also earned Foote the Writers Guild of America Award for Best Screenplay.

His other film scripts include Baby the Rain Must Fall starring Steve McQueen and Lee Remick, which was based on his play The Travelling Lady. The film was directed by Robert Mulligan who had worked with Foote on To Kill a Mockingbird a few years earlier.  Foote generally wrote screenplays that were based on his plays, such as the semi-autobiographic trilogy of 1918 (1985), On Valentine’s Day (1986) and Courtship (1987). 1918 and On Valentine’s Day were shot on location in Waxahachie, Texas. His screenplay for The Trip to Bountiful (1985) attracted another Academy Award nomination with Geraldine Page winning an Academy Award for Best Actress..

He also adapted works by other authors, such as John Steinbeck (Of Mice and Men directed by and starring Gary Sinise with John Malkovich). In addition to Faulkner’s “Old Man”, he also adapted Faulkner’s short story “Tomorrow” into a 1972 film starring Robert Duvall. Foote had previously adapted the story into a play. Leonard Maltin, in his movie guide book, calls the movie the best film adaptation of any of Faulkner’s work. On the subject of Faulkner, Foote said, “Faulkner I never met but evidently he liked [my adaptations] because he’s allowed me to share the dramatic copyrights to both Old Man and Tomorrow … So in other words, you have to get both our permissions to do it.”  Playwright Lillian Hellman adapted his play for the 1966 film The Chase with Marlon Brando, Jane Fonda and Robert Redford.  Foote provided the voice of Jefferson Davis for Ken Burns’ critically acclaimed documentary “The Civil War” (PBS, 1990), and adaptations of his plays “The Habitation of Dragons” (TNT, 1992) and “Lily Dale” (Showtime, 1996) preceded the Showtime production of “Horton Foote’s Alone” (1997).

Foote’s final work was the screenplay for Main Street, a 2010 drama film starring Colin Firth, Patricia Clarkson and Orlando Bloom.  Foote was awarded an honorary doctorate from Carson-Newman College. He also received an honorary doctorate of humane letters from Spalding University, Louisville, Kentucky, in 1987. One of Foote’s primary biographers is Dr. Gerald Wood, chair of the English Department at Carson-Newman College. Books by Wood about Foote include Horton Foote and the Theater of Intimacy and Horton Foote: A Casebook. Baylor University also holds close ties with Foote. In 2002, Horton Foote accepted the title as “Visiting Distinguished Dramatist” with the Baylor Department of Theatre Arts.

Foote was the cousin of actor/director Peter Masterson who directed three of his screenplays, including The Trip to Bountiful, Convicts and the Hallmark Hall of Fame television production of Lily Dale, starring Mary Stuart Masterson, Peter’s daughter. Foote was the third cousin of Shelby Foote, an American historian and novelist who wrote about the Civil War and who appeared in Ken Burn’s PBS documentary The Civil War in 1990.  Tess Harper, an actress who worked with Foote on Tender Mercies, described him as “America’s Chekhov. If he didn’t study the Russians, he’s a reincarnation of the Russians. He’s a quiet man who writes quiet people.” Regarding his own writing, Foote said, “I know that people think I have a certain style, but I think style is like the color of the eyes. I don’t know that you choose that.”  Foote was married to Lillian Vallish Foote (July 1923 – August 1992) from 1945 until her death. Their four children are actors Horton Foote, Jr. and Hallie Foote, playwright Daisy Brooks Foote, and director Walter Vallish Foote. All have worked on projects with their father. Horton Foote was introduced to Christian Science while in California and went on to become a dedicated member of the church. He served as a First Reader in a branch church in Nyack, N.Y., and also taught Sunday School for many years while living in New Hampshire.

Foote was the voice of Jefferson Davis in the 11 hour PBS series “The Civil War”. Shelby Foote wrote the comprehensive three volume, 3000-page history, together entitled The Civil War: A Narrative upon which the series was partially based and who appeared in almost ninety segments. The two Footes are third cousins; their great-grandfathers were brothers. “And while we didn’t grow up together, we have become friends; I was the voice of Jefferson Davis in that TV series,” Horton Foote added proudly.  Horton Foote made an effort to employ lifelike language in his writing, citing W. B. Yeats’ work as an example of this realistic approach. In an interview with playwright Stuart Spencer, Foote discusses his writing and material: “I think there’s certain things you don’t choose. I don’t think that you can choose a style; I think a style chooses you. I think that’s almost an unconscious choice. And I don’t know that you can choose subject matter, really. I think that’s almost an unconscious choice. I have a theory that from the time you’re 12 years old all your themes are kind of locked in.”.