[8] It is also served by metropolitan rail services, operated by Metro Trains, and connects with Flinders Street station and the underground City Loop.

In the 1880s, it was proposed that Spencer Street station be removed in order to facilitate the westward expansion of the city, but the plan was subsequently rejected.

[17] The viaduct to Flinders Street was expanded to four tracks in 1915[20] and, following the electrification of the suburban lines through the station, today's platforms 11 to 14 were opened in 1924, along with a pedestrian subway providing access to them.

[21][17] In 1938, it was announced that construction of an improved station entrance and new car park had been approved, designed by architects Messrs Stephenson and Meldrum, costing £2,000.

In 1960, work started on a new Spencer Street station, as part of the construction of a new interstate standard gauge line to Sydney, New South Wales.

During radical redevelopment (2002–2006) Freedman's mural was removed,[26] but due to bargaining by the CFMEU,[27] it remains on display above shop-fronts in the adjacent retail centre, DFO.

[27] Southern Cross was redeveloped by the Civic Nexus consortium, following an innovative design by Grimshaw Architects and Jackson Architecture which features an undulating roof.

This new shopping complex originally comprised a Direct Factory Outlet centre, a Virgin Megastore, along with food courts.

In 2009 the DFO relocated to a new site at South Wharf, the shopping centre being refitted by owner Austexx and rebranded simply as "Spencer Street fashion station".

[32] Complaints about access to platforms, empty trains occupying space during the day and lack of government support were raised by Leighton Contractors, the construction firm overseeing the project.

This led to concerns that the station might not be ready in time for the Commonwealth Games, and the government arranged with the railway operators to provide more access to the work site.

The station has been awarded the Royal Institute of British Architects' Lubetkin Prize for most outstanding building outside the European Union.

For all suburban and some country services, passengers using the main entrance on the corner of Collins and Spencer Streets have to ascend two escalators to a shopping concourse and then enter the paid area of the station, before descending again to the metropolitan platforms.

Local architects have cited some of the Southern Cross station's shortcomings: the building's poor connection to the surrounding streets; its awkward juncture at the pedestrian bridge that links Spencer Street to Docklands Stadium; and the baffling manner in which the grand architectural gesture of Southern Cross Station tapers off into an uninspired homage to the boxy 1980s shopping centre—Spencer Outlet Centre.

[37] In 2024, air quality data for Southern Cross station was released for the first time, showing that nitrogen dioxide levels have exceeded the World Health Organization's guidelines by 90 times; respiratory experts stated that both short-term and long-term human health is put at risk due to the high air pollution, which is caused by diesel emissions from regional trains and coaches at the station.

These platforms allow trains to avoid the North Melbourne Flyover, which is an inconvenience for trains as it has a maximum speed of 15 km/h (9.3 mph), and has shown to cause abnormal wheel wear on the VLocity fleet, as confirmed by an independent report commissioned by V/Line in 2016 to find out the cause of the problem, which ultimately led to up to a month of cancellations of services.

The clock was extensively restored before its return to Southern Cross, but the original mechanism remains in the collection of Museum Victoria.