The station was opened on 10 January 1863 as the terminus of the original Metropolitan Railway, the world's first underground metro line.

It was renamed Farringdon & High Holborn on 26 January 1922 when the new building by the architect Charles Walter Clark[10] facing Cowcross Street was opened, and its present name was adopted on 21 April 1936.

It retains indications of the Metropolitan Railway's main-line style operation such as a sign for a parcel office on the outer wall and some original signage, with the 1922–1936 name on the facade.

Farringdon has recently received significant upgrades to allow it to meet the needs of a series of major rail upgrade projects: The Thameslink Programme was a major upgrade to the existing north-south Thameslink route, enabling longer and more frequent trains, completed in 2018; and the Four Lines Modernisation involves the wholesale resignalling of the London Underground's sub-surface lines bringing a major boost in capacity to Circle, Hammersmith & City and Metropolitan line services calling at Farringdon.

Once all these projects have been completed, Farringdon will be one of the country's busiest stations with approximately 200 tph, an average of one departure every 20 seconds.

[17] The existing station building has been refurbished with a new roof canopy covering the north end of all four platforms and a new entrance and concourse facing Turnmill Street.

An additional ticket hall has been built on the south side of Cowcross Street providing access to the Thameslink platforms, which have been extended southwards underneath this building, allowing the station to handle 240 m (12-carriage) trains.

[21] It was necessary to build the Thameslink platform extensions to the south, since there is a sharp gradient to the immediate north of the station.

[22] The platform extensions cross the former Moorgate line and reach within a few metres of the entrance of the Snow Hill Tunnel.

[27] From 24 May 2022 the new railway line linked Farringdon to Abbey Wood via Canary Wharf in the east and Paddington, in the west.

Consisting of the letters of the alphabet in wood type set in Johnston, the memorial was unveiled by Sir Peter Hendy in 2019.

[33][34] At the western entrance, the glazing alongside the escalators are printed with giant diamonds, referencing the jewellers located nearby in Hatton Garden.

[33][34] The London Underground part of the station is directly next to the Thameslink platforms and is served by the Metropolitan, Hammersmith & City and Circle lines, between King's Cross St Pancras and Barbican.

[45] Prior to 2009, Thameslink services also ran to Moorgate via Barbican with trains diverging from the core route east of the platforms at Farringdon.