Culver Tunnel is on the disused Teign Valley railway line which ran between Heathfield and Exeter. The Teign Valley line was given Royal Assent in 1863 and opened in October 1882. The original track ran from the Moretonhampstead and South Devon Railway at Heathfield as far as Christow. Although authorised as broad gauge, it was built to standard gauge – this decision meaning that through traffic past Heathfield was not initially possible as the GWR line there was still broad. The line was primarily built to service mineral (mainly granite) traffic but a passenger service was also run.
The Exeter, Teign Valley and Chagford Railway was formed to complete the connection between Christow and Exeter but this link was not completed until 1903. This connection meant that the line also provided an alternate through route to Cornwall, by-passing the exposed seawall section of the mainline at Dawlish. In a total length of around 17 miles, the branch has two tunnels. These were apparently built in order to hide the trains from the view of Edward Byron of Culver House. To the south west of Longdown station is the 248 yards Culver tunnel.
The railway became part of the Great Western Railway in 1923. Passenger services lasted until 1958 when they were withdrawn by the British Transport Commission, anticipating Beeching by five years. Longdown Station was closed at the same time and offered back to the original landowners as per the conditions of the original sale.