Watford Stadium station did not come into existence until 1982, 70 years after the branch had been opened. It was built to serve Vicarage Road Stadium as a means of managing the crowds attending football matches; prior to this, the nearest stations available to football fans were Watford High Street and Watford Junction. A direct transport connection from the stadium would enable football officials to keep fans of "away" teams separate from Watford F.C. supporters and reduce instances of football hooliganism in Watford town centre. The station acquired the nickname of "Hooligan Halt".
Development of the station was funded jointly be the Football Trust, which contributed £50,000, Watford Borough Council (£80,000), Watford F.C. (£50,000), with the remaining £200,000 paid by British Rail. It was officially opened on 4 December 1982 by the rock musician and chairman of Watford Football Club, Elton John, and chairman of the Football Trust, Lord Aberdare. The inaugural train rolled into the station 5 minutes late. The station was only open on match days, with the first crowds passing through the station being Manchester United fans on the opening day.
The Croxley branch was temporarily closed in 1996 when a local road construction scheme severed the line and formal closure of the line was enacted in 2001. However Watford Stadium Halt had not been used for some years prior to this although it is not know exactly when the Halt was last used. The Halt was not demolished and the station furniture, including the lampposts and signage, was left in situ and despite nature reclaiming the station, the platforms and station furniture, apart from the station nameboards, were still in place when clearance work in preparation for the building of the Croxley Rail Link began in 2014. When the station is finally demolished it will have been abandoned for longer than the total length of time that it was in use.