The station was constructed by mining methods, and has four levels to a maximum depth of 32 metres. The site was a geological "sandwich" of basalt in the arch area, Silurian mudstone bedrock in the lower half, and silt in the middle, which precluded the construction of lower and upper platforms as separately driven tunnels.^[6]

Instead, the station platforms consist of two chambers linked by cross tunnels, each having two platforms on top of each other. The side of each chamber was made up of two drift tunnels, one at the top and one at the bottom. These were then linked together by 228 vertically raise bored shafts, 1 metre in diameter and 3 metres apart. The shafts and drifts were then filled with concrete, and formed the side skeleton of the station chambers. The arch of each chamber was then constructed underground across the top of the two side walls, the material below the arch excavated down to the bottom of the side walls, and temporary cross struts added between the raise bored columns until the permanent elements were added. This innovative method resulted in a $1 million saving in construction costs.^[7]

Flagstaff was the last station on the loop to open. Although trains had run through the station site since 24 January 1981 when the City Loop began operating, Flagstaff only opened to passengers on 27 May 1985.^[8][9] Initially, the City Loop did not operate at all on Sundays. That was changed with the introduction of Sunday trading, but at the same time that the other two underground loop stations opened on Sundays, Flagstaff station had its Saturday services cancelled.^[10]

In May 2017, CDC Melbourne operates one route 605 to Gardenvale from Flagstaff Station.

The station is located under the intersection of La Trobe and William streets and has two entrances – via lift or escalator south of La Trobe Street, and by stairs on the north. Flagstaff has three underground levels. The concourse level has a ticket office, ticket operated gates, toilets, a news stand and a hot snack shop. Flagstaff's four platforms are on the two levels below, with each level having an island platform. The levels are linked by elevators, 14 escalators and stairs.^[7] The four platforms serve a separate group of rail lines that leave the loop and radiate out into the city's suburbs.

In October 2012 it was revealed that traders and residents in the north-west area of the Melbourne CBD had begun a campaign to have Flagstaff station opened on weekends, arguing that its closure had a deadening effect on the life of the area. A petition calling for the station's weekend opening, only collected about 150 signatures in the first week.^[10]

With a number of residential developments having been built, the station was scheduled to open on weekends from June 2015, with both political parties having committed to this in the 2014 State Government Election.^[11] This was however deferred until January 2016.^[4][5]

  Media related to Flagstaff railway station at Wikimedia Commons

• Melway map at street-directory.com.au