Atherton was successful on the New York stage immediately after graduating and worked with many of the country's leading playwrights including David Rabe, John Guare, and Arthur Miller, winning numerous awards for his work on and off Broadway.[4]
Atherton also starred as cowboy Jim Lloyd in the miniseries Centennial (1978), based on the novel by James Michener. He appeared in the comedy Ghostbusters (1984) as the officious and condescending EPA agent Walter Peck.
Martha Coolidge chose Atherton to play Professor Jerry Hathaway in the teen comedy Real Genius (1985). Atherton played reporter Richard "Dick" Thornburg in the blockbuster action film Die Hard (1988), and reprised the role in its sequel Die Hard 2 (1990).[9]
Atherton was cast in the final season of ABC's Lost.[11] He appeared in the musical Gigi for the Reprise Theatre in Los Angeles as "Honoré Lachailles" in 2011.[12]
In summer 2014, Atherton was cast in a recurring role as Viceroy Mercado in the Syfy series Defiance's second season.
Atherton co-starred in the 2017 Netflix thriller, Clinical,[15] and appears in several upcoming documentaries on his most iconic films. The first to be released is the 2019 Cleanin' Up the Town: Remembering Ghostbusters which features the original 1984 cast.[16]
Atherton has sung in various productions in later years. In 2011, he performed "I Remember It Well," a popular song from Gigi with his former Reprise Theater co-star, Millicent Martin, at a sold-out performance in Palm Springs for Michael Childers' One Night Only, benefiting the Jewish Family Service of the Desert.[19] He returned in 2013 to the same sold-out event to sing the classic, "Isn't It Romantic?"[20]
Atherton appeared with his former Centennial costar Stephanie Zimbalist in the Gregory Peck Reading Series, a project of the Library Foundation of Los Angeles benefiting the Los Angeles Public Library. Roddy McDowall was host for the event.[21]
In December 2018, Atherton participated in the Library Foundation's reading of excerpts from book editor and critic, David Kipen's best-seller, Dear Los Angeles: The City in Diaries and Letters, 1542 to 2018.[22]