Arunoday Singh made his debut with Sikandar (2009), directed by Piyush Jha, playing a Kashmiri terrorist. His second film was Anil Kapoor's home production Aisha (2010), an adaptation of the novel, Emma by Jane Austen, with Sonam Kapoor. Also in the same year, he appeared in Vinay Shukla's take on Gender and sexuality in Mirch, through a collage of five stories, with Raima Sen and Konkana Sharma, where he played the central character of a struggling film director.
In 2011, he acted alongside Irrfan Khan and Aditi Rao Hydari, another newcomer in Sudhir Mishra's Yeh Saali Zindagi (2011). His performance earned him a nomination for Best Actor in a Supporting Role at the 18th Screen Awards. He next appeared in Jism 2 opposite Sunny Leone and Randeep Hooda. In 2014 he appeared in David Dhawan's comedy film Main Tera Hero opposite Varun Dhawan, Ileana D'Cruz and Nargis Fakhri; and the supernatural thriller film Pizza. His next release was Mr. X as Dr. Steve Rhodes opposite Emraan Hashmi and Amyra Dastur. In 2016, Singh appeared in Ashutosh Gowariker's epic-adventure romance film Mohenjo Daro, alongside Hrithik Roshan and Pooja Hegde.
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