Glenne Headly, who has died aged 62 from complications after a pulmonary embolism, was a gifted, sympathetic actor equally accomplished at comedy and drama. She was widely loved for her jaunty turn in Dirty Rotten Scoundrels (1988) as the soft-hearted dope targeted by two Côte d’Azur conmen, played by Michael Caine and Steve Martin.

Headly pulled off the difficult task of seeming oblivious to their tricks without appearing witless. In the film’s final moments, she turned the tables on her would-be exploiters in a satisfying switcheroo that Headly had helped cook up when the scripted ending proved inadequate. The director, Frank Oz, was pleasantly surprised. “People so far – and in a way I almost did it myself – have just been scratching the surface of her talent,” he said at the time.

Her breezy air positively invited people to underestimate her, while a high, breathy voice and ditsy mannerisms earned her comparisons with Judy Holliday; she even appeared on stage as the uneducated ex-chorus girl Billie Dawn, the part originated by Holliday, in a 1988 production of Born Yesterday. “Glenne certainly has a Judy Holliday quality,” noted Caine, “but she can do so much more.” Her friend and fellow actor Susan Berman warned against taking Headly at face value. “Because of her voice and her spontaneity, the way she’ll say whatever pops into her head in this innocent-little-girl voice, people sometimes think she’s this quirky scattered ingenue who has to be protected,” she said. “But anybody who knows her knows she’s incredibly smart and principled and independent. No one needs to take care of Glenne.”

She was born in New London, Connecticut, and lived in various locations as a child, including Florida, San Francisco and the Philippines, owing to her stepfather’s job as a naval intelligence officer. When Glenne was four, her mother, Joan Ida Sniscak, divorced her stepfather and moved with her to New York City. After showing youthful promise as a comic performer, she enrolled at the High School of Performing Arts and later worked as a waitress in the same diner as Ellen Barkin while both women were trying to get acting gigs. “Ellen yelled at the customers who weren’t nice to me,” she later recalled.

Facebook Twitter Pinterest Glenne Headly in ER in 1996. Photograph: NBC/Getty

When she failed to get any crumbs of work in New York, Headly decamped to Chicago where she fell in eventually with the Steppenwolf Theatre Company. There she met John Malkovich, whom she married in 1982. (The couple divorced six years later.) She worked in the costume department while receiving glowing notices in company productions staged in New York, including Arms and the Man, with Kevin Kline and Raúl Juliá, and Balm in Gilead, both directed by Malkovich.

She also began appearing in films, with small parts in Woody Allen’s The Purple Rose of Cairo (1985), the drama Eleni (1985), alongside Malkovich, and the science-fiction comedy Making Mr Right (1987). She played the mother of a girl whose drawings come to life in the British horror Paperhouse (1988), in which she dubbed her own performance at the 11th hour when the film-makers decided she should have an English accent. Her profile was greatly increased by Dirty Rotten Scoundrels and by the popular television miniseries Lonesome Dove (1989), in which she played a sheriff’s wife who falls in with a band of buffalo hunters. She earned an Emmy nomination for that, as well as for Bastard Out of Carolina (1996), a drama about child abuse directed by Anjelica Huston.

In Warren Beatty’s Dick Tracy (1990), she was a palpably human presence in a film dominated by pop-art production design and synthetic comic-strip colours. She did strong work as a woman suspected of killing her abusive husband in Alan Rudolph’s Mortal Thoughts (1991) and turned up in the same director’s patchy adaptation of Kurt Vonnegut’s Breakfast of Champions (1999). She had a recurring role in 1996 on the medical drama ER, but few of the other parts she received subsequently were worthy of her. She was a detective in the unappealing Macaulay Culkin comedy Getting Even With Dad (1994) and the wife of an inspirational music teacher, played by Richard Dreyfuss, in the schmaltzy Mr Holland’s Opus (1995). She was reunited with Steve Martin, less happily this time, in Sgt Bilko, a blundering 1996 film version of the Phil Silvers sitcom.

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More recently, she starred in the comedy Don Jon (2013) as the mother of the porn-addicted hero and alongside Tom Hanks and Emma Watson in the internet thriller The Circle (2017). She will shortly be seen in the crime comedy Villa Capri with Morgan Freeman and Tommy Lee Jones. On television, she played a lawyer in The Night Of (2016), the HBO adaptation of the BBC series Criminal Justice, and had not yet completed a new TV comedy, Future Man, at the time of her death.

She is survived by her mother, her second husband, Byron McCulloch, whom she married in 1993, and their son, Stirling.

• Glenne Aimee Headly, actor, born 13 March 1955; died 8 June 2017