The station opened on 31 July 1933, the last of the stations on the extension of the line from Finsbury Park to do so and four months after Oakwood station opened. Prior to its opening, "Trent Park" and "Cock Fosters" (an early spelling of the area's name) were suggested as alternative station names. The original site hoarding displayed the name as a single word.
The station was designed by Charles Holden in a modern European style using brick, glass and reinforced concrete. Compared with the other new stations Holden designed for the extension, Cockfosters' street buildings are modest in scale, lacking the mass of Oakwood or Arnos Grove or the avant-garde flourish of Southgate. The most striking feature of the station is the tall concrete and glass trainshed roof and platform canopies which are supported by portal frames of narrow blade-like concrete columns and beams rising from the platforms and spanning across the tracks. The trainshed roof constructed at Uxbridge in 1937-38 was built to a similar design. Cockfosters station is a Grade II listed building.
The station has three tracks with platforms number 1 to 4; the centre track being served from both sides by platforms 2 and 3. Most northbound Piccadilly trains terminate here although some terminate at Oakwood or Arnos Grove, particularly in peak hours or in the evenings. Cockfosters depot is located between Oakwood and Cockfosters and trains can access or leave it from either direction.
In late 2006, Cockfosters Station began an intensive refurbishment programme to bring it up to standards with all other stations on the Tube network, as part of the Tube's £10billion upgrade scheme. The aim was to modernise the area, but still maintain the charm of the old building.
The plans included:
Resurfacing the staircase on the East and West entrances to make them more user-friendly for those with sight problems.
Painting of the original wooden seating areas on the East side entrance as well as minor restoration.
Fitting of "Emergency Signal" notices on either side of the station to alert passengers of closed entrances.
Installation of electronic platform train schedule systems, which inform passengers of immediate tube departures in addition to the destination. This aims to reduce confusion as to which of the three tube platforms' trains will be leaving first, and when.
Installation of full CCTV operation both above and below the station grounds to improve security.
Installation of London Underground Passenger Information systems, both above and below ground
The above improvements were made to the station as well as a number of more minor additions to improve the building and bring it up to modern-day usage standards.
Cockfosters tube station features prominently in the novel While England Sleeps by American author David Leavitt. One of the novel's protagonists is writing a book entitled The Train to Cockfosters.