Drayton Park station was opened by the Great Northern & City Railway (GN&CR) on 14 February 1904. The GN&CR was established to create a route for Great Northern Railway (GNR) trains between Finsbury Park and the stations of the Metropolitan Railway (MR) and City & South London Railway at Moorgate. Except for Drayton Park station and the former depot, which are located in a deep cutting, the railway was constructed as a tube tunnel. The tunnels were designed with a larger diameter than other deep-tube railways to accommodate GNR main-line trains. A disagreement between the two companies prevented the GN&CR from connecting its tunnels to the GNR platforms at Finsbury Park. As a result, the GN&CR tunnels terminated beneath the main-line station without a direct surface connection. Rolling stock accessed the line through a yard connection at Finsbury Park.

In 1913, the MR took over the GN&CR, and the line operated under the MR name until it became part of the London Passenger Transport Board (LPTB) in 1933. In preparation for the LPTB’s Northern Heights plan, the line was transferred to the control of the Morden-Edgware Line, now known as the Northern Line.

The Northern Heights plan involved constructing the GN&CR’s unbuilt connection from Drayton Park to the surface platforms at Finsbury Park and transferring the London and North Eastern Railway (LNER) branches from Finsbury Park to Edgware, High Barnet, and Alexandra Palace. By 1939, much of the work for connecting the lines had been completed, including the necessary ramps to take the tracks from Drayton Park up to Finsbury Park. The opening of the connection was scheduled for autumn 1940, but the outbreak of the Second World War halted further construction.

After the war, the plan to incorporate the Alexandra Palace branch into the Underground was abandoned, and it ceased passenger services in the 1950s. No further attempts were made to connect the City Line to the main-line platforms, owned by British Railways after nationalisation in 1948, and Northern Line tube trains continued to operate in tunnels to Finsbury Park.

Although the Victoria Line does not serve Drayton Park, its construction in the 1960s had a significant impact on the station. The City Line tunnels north of Drayton Park were closed on 3 October 1964 and repurposed for the Victoria Line, which connected to them south of Finsbury Park. Drayton Park became the northern terminus of the City Line, later known as the Northern Line Highbury Branch.

On 4 October 1975, the line closed and ceased to be part of the London Underground. It was transferred to British Rail (BR), and the unused ramps from the canceled Northern Heights plan were finally fitted with tracks to connect the line to the surface platforms at Finsbury Park. On 8 August 1976, Drayton Park reopened as part of the BR network, with main-line-sized trains operating to Old Street. On 8 November 1976, 72 years after the GN&CR’s opening, the line was opened for main-line trains from Moorgate to Finsbury Park and beyond, as originally intended.

Following the transfer of the line from London Transport to British Rail, the tube train car sheds at Drayton Park became redundant. The tracks in the sheds and yard, which had been used only by slow-moving empty tube trains, were in excellent condition. They were purchased by the Ffestiniog Railway in North Wales, and the task of lifting and loading them onto a bogie flat wagon was carried out