Born to Tamil film director and producer Kasthuri Raja, Dhanush entered acting after being pressured by his brother, director Selvaraghavan. Dhanush married Aishwarya (who is almost 19 months elder), Rajinikanth's daughter on 18 November 2004. They have two sons named Yatra and Linga who were born in 2006 and 2010. He studied at the Thai Sathiya Matriculation High School, Saligramam from Kindergarten (also known as LKG - Lower Kindergarten) to SSLC (also Known as 10th Std.) and St. John's Matriculation Higher Secondary School Alwarthirunagar and shifted to JRK Matriculation Higher Secondary School in Vadapalani, Chennai for attending 12th State Board Exams for last one and half months due to lack of permission for attending Exam from previous School.
Dhanush debuted in the film Thulluvadho Ilamai, directed by his father Kasthuri Raja, which received mostly positive reviews from critics and the public. He then appeared in his brother Selvaraghavan's first directorial venture, Kadhal Kondein. The film portrayed Dhanush as a mentally-disturbed youth, Vinodh, who yearned for the love of his friend, eventually turning possessive over her. Upon release, the film won critical acclaim and also became a major commercial success. His next film, released later in 2003, was Thiruda Thirudi.
Dhanush appeared in Pudhukottaiyilirundhu Saravanan and Ramana's Sullan. Later, he also appeared in Dreams, another film panned by critics. The film was directed by his father, like their previous ventures. In 2005, Dhanush appeared in Devathaiyai Kanden. Later it was dubbed into Telugurert, and in very same year he also worked on Balu Mahendra's Adhu Oru Kana Kaalam.
Pudhupettai re-united Dhanush with his brother. Dhanush's portrayal was praised by critics. The Telugu dubbed version was titled Dhoolpet. Dhanush went on to star in the commercial entertainer Thiruvilayadal Arambam romancing Shriya Saran.
Dhanush's first release of 2007, Parattai Engira Azhagu Sundaram did not go well. The film, which was a remake of the successful Kannada language film, Jogi'. However, his second film Polladhavan was released during Diwali 2007. Polladhavan was based on 1948–Italian neorealist film The Bicycle Thieves and Dhanush's performance was appreciated.
The remake of a Telugu film directed by his brother formed the plot line for Dhanush's next movie directed by debutant Mithran Jawahar. The movie titled Yaaradi Nee Mohini. He later appeared in a cameo appearance, for his father-in-law Rajinikanth's venture, Kuselan. His subsequent venture was Suraj's Padikathavan which was released in January 2009. His performance was praised and well received. His next two films Kutty and Uthama Puthiran, were both collaborations with director Mithran Jawahar.
Dhanush's first release in 2011, which he had shot for over three years, was Aadukalam, marking his second collaboration with Vetrimaran. Dhanush played the role of a local cockfighter and described the venture as his "Dream Project" during production. The film gained highly positive reviews and won six awards at the 58th National Film Awards, with Dhanush receiving the National Film Award for Best Actor, becoming the youngest actor to win the award. Dhanush appeared in an extended guest appearance in Subramania Siva's Seedan. His next two ventures were action-masala films: Mappillai, a remake of his father-in-law's same-titled 1989 film and Venghai, by Hari, which received mixed reviews but was a commercial success.
Dhanush's next film, Mayakkam Enna, in which he again collaborated with his brother, casting him with Richa Gangopadhyay, received largely positive reviews. His only 2012 release was 3 directed by his wife, Aishwarya Rajinikanth with Shruti Haasan. The movie was a moderate success, owing to the popularity of the song Why this Kolaveri Di. In 2013 he appeared in Maryan opposite Parvathi Menon, which was applauded by critics but became an above-average grosser at the box office. His next release was Naiyaandi, directed by A. Sarkunam, which did not make any notable impact in the box office.
Dhanush's first film of 2014 was Velaiyilla Pattathari, which was also his 25 film and was directed by Velraj. It received mostly positive reviews and was a success. His next release was Shamitabh, released in year 2015 which was also his second Hindi film directed by R. Balki opened to very high positive reviews and was praised for the concept but failed at box-office. His next film Anegan was a psychological thriller directed by KV Anand which generated positive reviews and became a box office success.
Dhanush's next release in 2015 was the action comedy Maari, featuring Kajal Aggarwal, Robo Shankar, and Vijay Yesudas. Directed by Balaji Mohan and composed by Anirudh, it was released worldwide on 17 July 2015. He also appeared in Thanga Magan directed by Velraj with Samantha Ruth Prabhu, Amy Jackson, K. S. Ravikumar and Raadhika Sarathkumar.In 2016, Dhanush appeared Thodari which was a raailroad disaster film and Kodi, a political thriller.
He played a cameo in his directorial debut Power Paandi, which released on 14 April 2017. Velaiilla Pattadhari 2, directed by his sister-in-law Soundarya Rajinikanth, will be his first film of 2017 as a lead actor. He has penned the story and dialogues for this movie and also produced it. Enai Noki Paayum Thota, directed by Gautham Menon and Vada Chennai are his other expected releases for this year. Dhanush has also signed on to appear in his first international film, titled The Extraordinary Journey Of The Fakir Who Got Trapped In An Ikea Cupboard, to be directed by Marjane Satrapi.
Dhanush occasionally records music, generally for his own films. He was introduced as a playback singer in Pudhukottaiyilirundhu Saravanan by its composer Yuvan Shankar Raja and collaborated again with him in his brother Selvaraghavan's directorial, Pudhupettai. He sang further numbers in Selvaraghavan's films Aayirathil Oruvan and Mayakkam Enna; the former featured him alongside his wife Aishwarya Rajinikanth.
"Why this Kolaveri Di" was released on YouTube in 2011 as part of the soundtrack to the film 3, the directorial debut of Aishwarya Dhanush. The song became the most searched video in India. Anirudh Ravichander was the soundtrack composer for the film and Dhanush wrote much of the lyrics. He has also sung "No Problem" in the Kannada movie Vajrakaya and "Thikka" in the Telugu movie Thikka.
Dhanush worked with WWF India to support Earth Hour 2012. In August 2013, Dhanush was signed by Perfetti India Ltd. as their brand ambassador for Center Fresh chewing gum.
He has made his directorial debut with the movie Power Paandi.
Dhanush has won or received nominations at the National Film Award, Filmfare Awards and Vijay Awards ceremony.