Angel Tompkins was a model in the Chicago area before being discovered by Woody Allen, who sent her to Universal Pictures. She was signed and became part of the last Universal Contract Players. She started her television and film-acting career in the late 1960s. She made her major film debut as the seductive blonde who came between husband and wife, Elliott Gould and Brenda Vaccaro, in the comedy I Love My ... Wife (1970) and was nominated for a Golden Globe. Tompkins was featured in the pictorial "Angel" in the February 1972 edition of Playboy; subsequently the magazine used her in three more editions, all presumably related to that film promotion.
On television, Tompkins appeared in the pilot for Search (1972, the pilot was originally titled "Probe", but the title name was changed to 'Search' due to a PBS program already having that title); she also appeared in several of the early episodes of 'Search'. She also appeared in many guest spots in shows such as The Wild Wild West (1965), Mannix (1967), Dragnet (franchise) List of Dragnet episodes (1967 series), 1969 episode "Forgery: (DR-33)"), Bonanza (1970), Police Woman (1970), Kojak (1977), The Eddie Capra Mysteries (1978), Knight Rider (1983), and Simon & Simon (1981). Tompkins additionally appeared in the episode "Gallery of Fear" on the Canadian sci-fi program The Starlost.
In 1987, Tompkins appeared in the comedy film Amazon Women on the Moon and with Ann-Margret in the film A Tiger's Tale, and made her last film appearances in Relentless (1989) and Crack House (1989). She also works in the commercial voice-over field.
In 1991, Tompkins was elected the national recording secretary of the Screen Actors Guild (SAG). She ran unsuccessfully for President of the guild in 1995. In 1996, she received the most votes for the SAG Hollywood Board of Directors. She ran for President again in 1999, changing her name to Angel Tompkins so that her name would appear first on the ballot, and came in third. In 2000, she proposed that members of SAG's partner union, American Federation of Television and Radio Artists, vote to decertify the union and recertify as part of SAG. She came in fourth in the 2001 SAG election, her fifth attempt.
