The station opened seven months after the railway line from North Melbourne was extended to Coburg,[4] and was named after the nearby bridge on Flemington Road that passes over the Moonee Ponds Creek.

[7] In 1891, the Parliamentary Standing Committee on Railways recommended the construction of a spur line from Flemington Bridge to Pascoe Vale, to relieve crowding on the Essendon line at peak times, as well as providing a shorter alternative route to the city, following the route of what is now CityLink.

The committee estimated the single track line would cost £93,000 to build, but recommended that only £30,000 be spent, with the remainder to be made up by donated land.

[7] In 1944, the current station buildings, with asbestos cement roofs, were provided and, at the same time, the stairs were replaced by asphalted ramps.

[7] In 1997, to allow construction of an elevated section of CityLink between Flemington Bridge and North Melbourne, a temporary crossover was provided near the Mount Alexander Road bridge, to allow Upfield line trains to terminate,[8] and passengers were shuttled by bus to Newmarket station to continue their journey.