Hughesdale station opened on 28 February 1925[4] and, like the adjoining suburb, was named in honour of James Vincent Hughes, mayor of Oakleigh from 1924 to 1925. He, with the Poath Road Railway Station League, had lobbied strongly for a new station for the area.[5] Before the station was built, Hughesdale had been the site of the junctions of both the Outer Circle and Rosstown lines with the Dandenong/Gippsland line.
In 1972, boom barriers replaced hand gates at the former Poath Road level crossing, which was located at the up end of the former ground-level station.[6]
In 1977, the former ground-level station building was rebuilt, after the original station building, which was of a timber construction, was destroyed by fire in 1975.[7][8]
In 2016, the Level Crossing Removal Authority announced a grade separation project to eliminate the Poath Road level crossing immediately to the west of the station. On 14 October 2017, the station was closed, and was demolished on 28 October of that year. On 25 August 2018, the rebuilt station opened about 250 metres (820 ft 3 in) west of the former station, as part of construction of the new section of elevated rail line between Caulfield and Oakleigh. As such, it is now located in the suburb of Murrumbeena rather than Hughesdale. [9]