On signing Rai, Dempo head coach at the time, Arthur Papas said "Vinit is a very cultured midfielder with a great range of passing.
[3] After spending a majority of the season playing for the club's youth team, Rai made his professional debut for Dempo in the league on 1 March 2015 against East Bengal.
[4] After helping Dempo regain promotion to the I-League, Rai signed with Indian Super League side Kerala Blasters on 6 September 2016.
In 2022, Rai was loaned out to Indian Super League defending champions Mumbai City from Odisha.
[9] Almost a year later, Rai made his debut on the bench for the India senior side in their FIFA World Cup qualifier against Iran.