Churston station was the location for the opening scene in "The System", a 1964 film. Several of the main characters arrive at the last minute and jump onto a Diesel Multiple Unit that is just pulling out towards Kingswear. After the opening credits, they then get off a different train at Brixham. Agatha Christie lived nearby at Greenway and set some stories in and around the area - Churston is the 'C' in the The A.B.C. Murders!

The Dartmouth and Torbay Railway from Paignton railway station to Churston was opened for passengers on 14 March 1861 and for goods traffic on 1 April 1861. The station was known as Brixham Road at the time, and the line was extended to Kingswear railway station on 16 August 1864. The initial single platform was supplemented by a second in 1865. The Dartmouth and Torbay Railway was always operated by the South Devon Railway Company and was amalgamated with it on 1 January 1872. This was only short lived as it was in turn amalgamated into the Great Western Railway on 1 February 1876.

In the meantime the station had changed its name to Churston when an independent branch line had been opened by the Torbay and Brixham Railway to serve the latter town on 28 February 1868. The station was now a junction but the goods shed had to be moved to a new site alongside the Brixham line to make room for a short bay platform to accommodate the Brixham trains. Sidings were added to allow for the goods traffic handled on the branch, including a busy trade in fish. The Torbay and Brixham Railway was taken over by the Great Western Railway on 1 January 1883.

The lines had been built using broad gauge, but on 21 May 1892 were closed for the weekend to be converted to standard gauge. The following year saw the platforms lengthened and a new signal box constructed. The platforms were further lengthened and a new signal box opened on 9 February 1913 to control the now extended crossing loop.

The Great Western Railway was nationalised into British Railways on 1 January 1948. The Brixham branch closed on 13 May 1963, but the Kingswear service continued but Sunday trains no longer called at Churston after the 1967 summer season. General freight traffic was withdrawn on 14 June 1965 although coal was still handled until 4 December 1967. The crossing loop was taken out of use on 20 October 1968 and the signal box closed.

The line was sold to the Dart Valley Light Railway plc on 30 December 1972 and since then Churston has become an important centre for engineering on the railway.

The signal box was reopened in 1979 and the following year the former Brixham bay platform was relaid. In 1981 the turntable from Goodrington was moved to a position alongside the Brixham junction at Churston. The signal box was closed again in 1991 when control of the whole line was transferred to Britannia Crossing at Kingswear. A locomotive workshop was built behind the Up (towards Paignton) platform in 1993 and the station building restored and reopened. The Brixham bay platform was then covered by a carriage workshop in 1996.