Opening one month after the railway line from Caulfield was extended to Oakleigh,[4] Murrumbeena station gets its name from Mirambena Road, its name believed to be derived from an Indigenousword meaning 'belonging to you', 'welcome', or 'land of frogs'.[5][6] The name may also refer to a member of the native police.[5][6]
A siding was once located at the down end of Platform 2. In 1972, it was reduced in length and,[4] in 1977, it was removed altogether.[4]
The station once had a signal box at the up end of Platform 1, which was removed in 1979, when boom barriers were provided at the former Murrumbeena Road level crossing, which was also located at the up end of the station.[7][8]
In March 2014, the Level Crossing Removal Authority announced a grade separation project to replace the Murrumbeena Road level crossing immediately to the west of the station, being done so as part of its elevated railway project. The historic station (protected by a local heritage overlay) and associated footbridge were removed and replaced with a temporary station until the completion of the project.[9] On 18 June 2018, the rebuilt station opened, with services commencing on the new elevated lines.[10]