A product of the Tata Football Academy, Rai kicked off his professional career through the ranks at Dempo before moving to the ISL with Kerala Blasters in 2016 and followed it with a loan stint at Minerva Punjab FC in the I-League. In 2017, the Assam-born midfielder made a move to Delhi Dynamos FC (later renamed Odisha FC) after being picked in the 2017 ISL Draft.