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In the 1990s, he mostly appeared in smaller roles in film, such as Outbreak (1995) and television. Dempsey was also in Scream 3 (2000) where he played the role of Detective Mark Kincaid.

He was successful in landing a lead role in Sweet Home Alabama (2002), a surprise box office hit. He has since starred in other films, including Brother Bear 2 (2006), Enchanted (2007), Made of Honor (2008), Valentine's Day (2010), Flypaper (2011), Freedom Writers (2007), Transformers: Dark of the Moon (2011), and Bridget Jones's Baby (2016).

Dempsey, who maintains a sports car and vintage car collection, also enjoys auto racing in his spare time. He has competed in pro-am events such as the 24 Hours of Le Mans, Rolex 24 at Daytona sports car race, and Ensenada SCORE Baja 1000 off-road race. Prior to the 2013 24 Hours of Le Mans, Dempsey declared that he would "walk away" from acting if he could and dedicate himself full-time to motorsports.