It was formed in 1965 as a merger of Leighton Buzzard and Linslade, which prior to 1965 had been administratively separate urban districts.

The name Leighton-Linslade is generally only used in a local government context as the name of the parish and its town council.

Following the completion of the Grand Junction Canal in 1800 and the opening of the London and Birmingham Railway in 1838, the area west of the River Ouzel between the canal and Leighton Buzzard railway station (both of which were in the parish of Linslade) began to be developed.

The River Ouzel provides the border between the parts, with Leighton Buzzard to the east and Linslade to the west.

The parish participates in international town twinning: The Leighton-Linslade Urban District Council created in 1965 inherited offices at 6 Leighton Road in Linslade from Linslade Urban District Council and at the White House, 37 Hockliffe Street in Leighton Buzzard from Leighton Buzzard Urban District Council.

The White House was used as the urban district council's main offices throughout its existence.

[12] The arms were transferred to Leighton-Linslade Town Council following local government reorganisation in 1974.