Huma Qureshi was initially scheduled to make her film debut with Billa II, a Tamil gangster-thriller, directed and produced by Chakri Toleti, after surviving an audition out of 700 candidates.
Huma Qureshi made her feature film debut with a supporting role in Anurag Kashyap's critically acclaimed two-part crime drama Gangs of Wasseypur – Part 1 (2012), where Qureshi was cast as the supportive wife of a criminal (played by Nawazuddin Siddiqui). She described her character as a small-town airhead who thinks she is the prettiest girl in the village: "Mohsina tries to copy everything she sees on the big screen in her own little ways. She is heavily influenced by Bollywood". Following the success of the first part, she reprised her role of Mohsina in the second instalment of the Gangs of Wasseypur series, Gangs of Wasseypur – Part 2. The film premiered in the Cannes Directors' Fortnight at the Cannes Film Festival with its prequel. It opened to wide critical acclaim, and her portrayal again received positive reviews.
That same year, Qureshi completed her three-film contract with Anurag Kashyap Films by starring in Luv Shuv Tey Chicken Khurana, a romantic comedy, which describes a quest for an ancient family dish; Chicken Khurana. Directed by Sameer Sharma, she played the role of a feisty Punjabi girl, Harman (star Kunal Kapoor's love interest). The film was a financial success, and Rediff.com noted that "Huma Qureshi looks right for the role and she delivers a wonderful performance".Aniruddha Guha of the Daily News and Analysis said: "[Qureshi], on the other hand, is charming as the fiery Punjaban, Harman. Her refreshingly natural acting style impresses again in a role that has shades of her character in Gangs of Wasseypur". However, Anupama Chopra found her performance to be "a little bland".
For her next feature, Qureshi was cast as a witch in the supernatural thriller Ek Thi Daayan (2013), alongside Emraan Hashmi, Konkona Sen Sharma and Kalki Koechlin.
She played the eponymous lead as a young girl who is struggling to come out of the clutches of her tormenting cousin brother (played by Satya Anand). The film was screened at Indian Film Festival of Los Angeles before its release and received generally positive reviews, and Qureshi's performance was critically acclaimed and earned her a Special Mention Award at the ceremony. Her subsequent release that year included the underworld drama D-Day, in which she was featured as Zoya Rehman, an explosive R.A.W agent with an ensemble cast including Irfan Khan, Arjun Rampal, Rishi Kapoor and Shruti Hassan. During the script narration, the director Nikhil Advani offered Qureshi the choice of which woman to play, either Suraiya (later played by Hassan) or Zoya; she decided on Zoya to expand her horizons as an actress. The film was a flop at the box office and received mixed feedback from critics, while Qureshi's performance received favourable reviews; Subhash K. Jha mentioned that Qureshi's acting is "effortlessly appealing and effective."
In 2014, Qureshi featured in Abhishek Chaubey's black comedy Dedh Ishqiya (2014), a sequel to the 2010 film Ishqiya, co-starring Madhuri Dixit, Arshad Warsi and Naseeruddin Shah . Dedh Ishqiya was a commercial success, earning ₹270 million (US$4.1 million) in India and abroad and Qureshi received praise for her portrayal of the promiscuous companion of a con woman (played by Dixit). In a 5-star review, Raja Sen commented that "Qureshi uses her fiercely intelligent eyes to great effect", whilst Mohar Basu agreed, saying that "Huma Qureshi is brilliant and confident.
The following year, Qureshi appeared as a prostitute in Sriram Raghavan's crime thriller Badlapur, alongside Varun Dhawan and Nawazuddin Siddiqui. Raja Sen praised her acting and wrote that she "is hauntingly good as a call-girl". The film was a commercial success, and Qureshi received the Filmfare Best Supporting Actress nomination. Umesh Kulkarni's Marathi film Highway marked her debut in Marathi cinema. It received mixed reviews from critics, and proved to be a moderate box office success.The same year, she acted in the collaborative film X: Past Is Present. It was directed by a team of eleven filmmakers with Qureshi appearing in "Knot", a segment directed by film critic Raja Sen, where she appeared alongside Anshuman Jha.
Qureshi's first release of 2017 was the courtroom comedy drama Jolly LLB 2, where she appeared alongside Akshay Kumar. A sequel to the 2013 film Jolly LLB, the film received mixed reviews from critics and was a box office success. Her next film was Gurinder Chadha's British-Indian historical drama Viceroy's House. The film follows the story of Viceroy's House in 1947 during the partition of India and was screened at the 67th Berlin International Film Festival. She then appeared along with her brother Saqib Saleem in Prawaal Raman's horror film Dobaara: See Your Evil (2017), a remake of Mike Flanagan's Hollywood flick Oculus (2013). Flanagan also served as the executive producer of the film.
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