Drayton Park was opened by the Great Northern & City Railway (GN&CR) on 14 February 1904.
The Northern Heights plan involved the construction of the GN&CR's unbuilt connection from Drayton Park to the surface platforms at Finsbury Park and the transfer of the London and North Eastern Railway (LNER) branches from there to Edgware, High Barnet and Alexandra Palace.
On 8 August 1976 Drayton Park reopened as part of the BR network, with main-line-sized trains running to Old Street.
Following the transfer of the line from London Transport to British Rail, the tube train car sheds at Drayton Park became redundant.
The job of lifting and loading it onto a bogie flat wagon fell to volunteers of the London Area Group of the Ffestiniog Railway Society.
Trains change between the two methods at Drayton Park and the transition may be noticeable as sparks or momentary power blackouts.
Great Northern introduced a weekend and late evening service from 13 December 2015, as part of their franchise requirements.