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Subsequently, she began to appear in supporting roles in films during the mid-1980s, achieving recognition in independent movies such as Promised Land (1988) before her performance in the Rob Reiner-directed romantic comedy When Harry Met Sally...

(1989) brought her widespread attention and her first Golden Globe nomination.

Several television films and smaller film roles followed, including appearances in Charles in Charge, Armed and Dangerous, Amityville 3-D and Promised Land; for her role in the lattermost she received her first Independent Spirit Award nomination. Her first leading role was the romantic comedy film When Harry Met Sally...

In the film, she portrayed the distraught wife of a kidnapped engineer, played by David Morse, while relying on a resourceful troubleshooter who makes a profession of dealing with international bandits.While the film became a lukewarm critical and commercial success, grossing million worldwide, it garnered much reportage in the tabloid press in association with Ryan and Crowe's affair.Also in 1994, Ryan won Harvard's Hasty Pudding Woman of the Year award, and People Magazine dubbed her one of "the 50 most beautiful people in the world." In 1995, critic Richard Corliss called her "the current soul of romantic comedy." That same year, she appeared opposite Kevin Kline in Lawrence Kasdan's French Kiss, a romantic comedy that catered to her "America's Sweetheart" image, and Ryan was awarded the Women in Film Crystal Award.(This award is given to "outstanding women who, through their endurance and the excellence of their work, have helped to expand the role of women within the entertainment industry.") In 1997, Ryan voiced the lead role in the animated film Anastasia, which garnered good reviews and enjoyed box office success.They had previously been paired as romantic leads in the film Joe Versus the Volcano—a commercial disappointment which later developed a cult following.

Hanks and Ryan would be paired for a third time in the film You've Got Mail.A year later, she once again returned to her romantic comedy roots with Kate & Leopold (2001), alongside Hugh Jackman.A film about a British Duke who travels through time from New York in 1876 to the present and falls in love with a successful market researcher in the modern New York, the James Mangold-directed film received a mixed-to-positive response, In 2003, Ryan broke away from her usual roles, starring alongside Mark Ruffalo and Jennifer Jason Leigh in Jane Campion's erotic thriller film In the Cut.After her film debut in George Cukor's Rich and Famous, Ryan played Betsy Stewart in the daytime drama As the World Turns, from 1982 to 1984, and her character was featured in a popular romantic story arc.Around that same time, she appeared in a Burger King commercial.During college, she acted in television commercials and the soap opera As the World Turns to earn extra money.