Duff's early career started by making guest appearances on made-for-television films such as True Women and on TV series such as The Amanda Show. In addition to guest-starring roles on Chicago Hope, Boston Public, and Third Watch, Duff became a familiar face starting in late 2002 as Amy Saunders/Sanders on the children's television series, Lizzie McGuire, which her sister Hilary starred in as the title role. In 2004, Duff made a guest appearances on That's So Raven as Katina Jones. After making guest appearances on television, Duff received her first role in a feature film when she was cast as Summer Wheatley in Napoleon Dynamite. The film earned her first Teen Choice Award win. She continued making guest appearances, which include Joan of Arcadia and American Dreams. She also lent her voice talent to the Christmas animation film In Search of Santa which again, featured sister Hilary. In 2005, Duff joined the cast of the television series 7th Heaven, playing Sandy Jameson, best friend to Simon's girlfriend Rose.

In June 2006, Duff joined the Broadway cast of Hairspray, portraying mean girl Amber Von Tussle, and left the role in early October 2006. Duff has also starred in Material Girls with sister Hilary, where she is credited as co-producer, with her mother and sister credited as producers. Following Material Girls, Duff appeared in various made-for-television or straight-to-DVD films including Nightmare, My Sexiest Year, Legacy, Backwoods, Love Takes Wing, Love Finds a Home and My Nanny's Secret.

Between 2008 and 2015, Duff appeared in various films and TV roles, including; Fear Island, Tug and Slightly Single in L.A.. She lent her voice to the animated film Foodfight!, but due to distribution issues, the film was delayed for years until it finally saw a release in 2012. Duff hosted the reality show Legally Blonde: The Musical – The Search for Elle Woods, which searched for an actress to take over the lead role in Legally Blonde: The Musical where she had been in the chorus. She was also listed as an executive producer of the series. Duff's most recent project was the film Badge of Honor in 2015.

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