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While studying at college, Nayantara was working as a part-time model. She was spotted by director Sathyan Anthikkad, who had seen some of her modelling assignments and approached her to play a pivotal role opposite Jayaram in his film Manassinakkare (2003). Although she turned down the offer initially, as she was not interested in films, she gave in eventually and agreed to do “just that one movie”.Manassinakkare went on to become a high financial success and she continued to receive acting offers. Her both releases in 2004, Natturajavu by Shaji Kailas and Fazil‘s pychological thriller Vismayathumbathu saw her co-starring alongside Mohanlal; while she played the protagonist’s adopted sister in the former, she portrayed a ghost in the latter. Her performance in Vismayathumbathu, in particular, was lauded, with critics claiming that she had “stolen the thunder with her author-backed role”, and was “the revelation of the film”. She also acted opposite Mammootty in Thaskara Veeran and Rappakal.
She subsequently started appearing in Tamil and Telugu films. In 2005, she was cast opposite Sarath Kumar in Hari’s Ayya, debuting in the Tamil film industry. The family drama film opened to positive critical response, fetching Nayantara positive feedback as well. Behindwoods.com claimed that she had made a “sensational debut in Tamil”, while a reviewer from Nowrunning.com said that her “presence with her beautiful smile is crowd winning”. While still shooting for Ayya, she was selected to portray the love interest of Rajinikanth in the comedy horror film Chandramukhi, after its director P. Vasu‘s wife had seen Manassinakkare and recommended her. The film became one of the most successful Tamil films in history, running for over 800 days in theatres, eventually turning Nayantara into one of the most-sought after actresses in Tamil. Later that year her third Tamil film, A. R. Murugadoss‘ Ghajini, in which she played a secondary female character, again was a commercially highly successful venture. However, she later told that appearing in Ghajini was a big mistake and the “worst decision” she ever took. Nayantara then accepted to appear in an item number as herself in the Perarasu-directed masala film Sivakasi starring Vijay.
Her first release in 2006 was Kalvanin Kadhali. Indiaglitz.com termed her performance as the “strength of the movie”. She next made her debut in Telugu, starring in the film Lakshmi, following which she performed in Boss, I Love You, alongside Venkatesh and Nagarjuna respectively. Three Tamil films in which she enacted the lead female characters – Vallavan, Thalaimagan and E – were released simultaneously during Diwali 2006. All three films opened to mixed reviews; Nayantara mostly won praise for her performances. In Vallavan, she portrayed a lecturer who falls in love with a student younger than her. Sify wrote: “Nayanthara virtually walks away with the film and has never looked so beautiful. She looks gorgeous especially in songs and does justice to her well-etched out role”. The science fiction thriller E featured Nayantara in the role of a bar dancer. Reviewers claimed that she made an impact, was “very adequate and impressive in a slightly complicated role”, and that she had “come up with a good performance”. In Thalaimagan, she played a news reporter, with critics agreeing that she did not have much to do in the film. She regained her star billing in Kollywood acting opposite Ajith Kumar in the Vishnuvardhan-directed gangster film Billa (2007). A remake of the same-titled 1980 Tamil film, it went on to become a blockbuster success at the box office, while Nayantara received many accolades for her performance as Sasha.Sify heaped praise on her, describing her as a “show stopper”. The reviewer further wrote: “Nayanthara has [...] go[ne] full throttle to look her sexiest best [...] She has a beautiful body which she flaunts daringly [...] and is also able to bring out the cold aloofness and bitterness of her character. Similarly a critic from Nowrunning.com noted that she looked “great in mini skirts, jacket, dark glasses and tall boots”.
In 2008 she had five releases, four of which were in Tamil. Her first release, the family entertainer Yaaradi Nee Mohini was critically acclaimed and one of the highest grossing Tamil films of the year. Nayantara’s portrayal of Keerthi was appreciated by critics. Behindwoods.com wrote: “Nayan dispels her bombshell act and proves that she can more than just that. She breaks into tears when needed, shows vicious contempt when rubbed the wrong way in the name of love, and looks endearing in songs”. Nowrunning.com cited that she “exhibits her acting skills in full measure [and] gives a moving performance in emotional scenes”, while Sify‘s critic wrote that she looked “sensational and has done a great job in perhaps the meatiest role she has done so far”. She won the Vijay Award for Favourite Heroine for second consecutive year, as well as a nomination for the Best Actress prize at the 56th Filmfare Awards South. Her subsequent releases, however, Kuselan opposite Rajnikanth, Sathyam opposite Vishal and Villu opposite Vijay, were all unsuccessful, while Aegan became an average grosser. Her only successful release in 2009 was Aadhavan with Suriya which released in October of that year.
In 2010, all her releases, which featured her as the female lead, turned out to be commercial successes. She delivered five super hit films in the four Southern languages – Bodyguard (Malayalam), Adurs and Simha (Telugu), Boss Engira Bhaskaran (Tamil) and Super (Kannada). She won the Asianet Film Award for Best Actress for her performance in Bodyguard. The latter three, in particular, were exceptionally successful, with Simha becoming one of the highest-grossing Telugu films of the year and Boss Engira Bhaskaran releasing to highly positive reviews and becoming a blockbuster.Upendra‘s Super, which marked her debut into the Kannada film industry opened to rave reviews, while her performance was also praised by critics. Her performances in Simha, Boss Engira Bhaskaran and Super eventually fetched her nominations for the Filmfare Best Actress Award in the respective languages. She also starred in Shyamaprasad‘s critically acclaimed Malayalam film Elektra. Her performance was well appreciated by critics when it was screened at the International Film Festival of India. The film was also screened at the Dubai International Film Festival. Her only release in 2011 was the mythological film Sri Rama Rajyam by Bapu, in which she played the role of Sita. The film was dubbed in the media as her swan song and considered to be her last release before her release as she was reported to quit acting thereafter. However, after her break-up with Prabhu Deva, she made a comeback; she began shooting for Krish‘s Krishnam Vande Jagadgurum in March 2012, following an 11-months sabbatical.
While shooting for her Tamil film Vallavan, she was romantically linked with the film’s director and co-actor Silambarasan Rajendar. She initially denied the reports. In November 2006, however, she confirmed that she and Silambarasan had broken up, going on to add that she will not work with him again. During the making, in 2008, and after the release of her film Villu, reports suggested that she was in a relationship with its director Prabhu Deva, with some sources even claiming that both had married secretly in June 2009. She had tattooed his name on her wrist, and began appearing with him in public, while keeping silence and refusing to comment about the issue, neither denying nor confirming the relationship. In September 2010 then, Prabhu Deva openly confessed his love for Nayantara and further stated that he would marry her soon. The issue soon gained media attention and turned into a controversy, since Prabhu Deva was already married and not divorced yet, with his wife Ramalath, unwilling to agree for a divorce, filing a petition at the family court, seeking directions against her husband and Nayantara from marrying, attending functions together and receiving awards as husband and wife and requesting a reunion with him. Furthermore, Ramalath threatened to go on hunger strike, if Prabhu Deva married Nayantara, while several women’s organizations also conducted protests against Nayantara for “bringing disrepute to Tamil culture”, burning an effigy of her. In 2012, Nayantara confirmed that she had ended her relationship with Prabhu Deva.