The first station simply known as Leighton was opened by the London and Birmingham Railway on 9 April 1838 as part of the first section of its line from to Denbigh Hall. The line had originally been planned to pass through Buckingham but opposition from the Duke of Buckingham ensured that it forced east through Linslade. A station with two-facing platforms was opened a ¼-mile south of the Linslade tunnels. These are arranged unusually for a four track main line: the southbound slow line has a tunnel to itself as does the northbound fast line, however the northbound slow and southbound fast lines share a tunnel. This stems from the fact that the line was built as double-track and when quadrupled, the two extra lines could only be placed along both sides, as single-track tunnels. In May 1848, the station became a junction when a branch line to Dunstable was opened. The London and North Western Railway replaced the first station in February 1859 by another more permanent structure located to the south. The new building had an imposing frontage featuring arched windows. Access to the Dunstable branch was controlled by Leighton No. 2 signal box situated to the north of the station, while the actual branch signals were controlled by the main line box to the south. In 1874, land was purchased to the south of the station alongside the Dunstable branch for the construction of goods sidings, which eventually became known as Wing Yard. The LNWR was absorbed by the London, Midland and Scottish Railway in the 1923 railway grouping and, in 1927, it added a crossover between the fast and slow lines. This was to play a significant role in the derailment of Royal Scot No. 6114 "Coldstream Guardsman" at Linslade on 22 March 1931 when the driver took the crossover at 50–60 mph instead of the regulation 15 mph. There had been a diversion in place on the fast lines and the driver had missed the warning signals. The engine overturned and six people were killed including the driver and fireman. The Scotland amateur football team was on the train, but remained unscathed. In 1957-8 the platform buildings were rebuilt and a concrete awning placed over the platform. At the entrance a larger booking / waiting hall, central heating, electric lighting and the cycle storage, parcels and loading bay were improved. The Great Train Robbery of 1963 occurred just south of this station, at near Ledburn, at a bridge on the southbound stretch towards Cheddington. Wing Yard was closed in February 1967 and it is now used as a car park, while the branch to Dunstable was closed from June. In 1989, the platforms were lengthened to accommodate 12-coach trains and a £1.8m project to rebuild the station was started.
The station is served by trains operated by London Northwestern Railway and Southern. The Monday-Saturday off-peak service is: ;London Northwestern Railway
There have been past proposals about reopening the route to Luton when little of it had been lost to new construction, as either a rail link or as a guided busway. Although there is now a guided busway between Dunstable and Luton, much of the Leighton Buzzard to Dunstable section was lost to the Leighton Buzzard Southern Bypass.
Accidents and incidents
On 22 March 1931, a passenger train was derailed due to excessive speed through a crossover. Six people were killed.
