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Nayanthara made her acting debut in the 2003 Malayalam film Manassinakkare with Jayaram.
She made her debut in Tamil cinema with Ayya (2005) and Telugu with Lakshmi (2006). After this she had numerous commercially successful Tamil and Telugu films like Chandramukhi (2005), Dubai Seenu (2007), Tulasi (2007), Billa (2007), Yaaradi Nee Mohini (2008), Aadhavan (2009), Adhurs (2010), Simha (2010), Boss Engira Bhaskaran (2010), Sri Rama Rajyam (2011), Raja Rani (2013), Arrambam (2013), Thani Oruvan (2015), Maya (2015), Naanum Rowdy Dhaan (2015), Babu Bangaram (2016) and Iru Mugan (2016), making her the highest paid actress in South India after Anushka Shetty.
She rose to prominence by featuring as the female lead in five of India's annually top-grossing romances—Yeh Dillagi (1994), Ishq (1997), Pyaar Kiya To Darna Kya (1998), Pyaar To Hona Hi Tha (1998) and Hum Aapke Dil Mein Rehte Hain (1999)—and received wide critical recognition for playing against type in the 1997 mystery film Gupt: The Hidden Truth, that earned her a Filmfare Award for Best Villain, and the 1998 psychological thriller Dushman.