Its first home was a disused cow byre which the group cleaned out and ran as the St. Andrews Play Club, giving performances to audiences who sat on cushions on the floor. Within a couple of years, the Byre Theatre had established a considerable reputation running a programme of performances which attracted audiences the theatre was barely able to hold.
In 1969, the original building was demolished to make way for a new housing development, and in 1970 the second building was opened. At a cost of £40,000, funded by a public appeal and the local authority, it was modeled on the Mermaid Theatre in London. The facilities were modest, for both public and staff, but it was thought to be rather grand compared to its predecessor.
A. B. Paterson's last ambition was yet again to modernise and refurbish the Byre Theatre to meet current expectations and requirements, in particular to address the inadequate facilities for those with special access needs, including visual or audio impairment.
At the time of his death in 1989, a proposal for expansion of the theatre's facilities had been initiated.
Today's Byre Theatre was built by award winning architects Nicoll Russell Studios of Broughty Ferry. The theatre grew from A.B. Paterson's aspirations for a truly modern theatre addressing the needs of the entire community.
The current building was opened in 2001 by Sean Connery. Its main auditorium is named A.B. Paterson, after the Byre founder. There is also a second 80-seat performance space named after the late golf photographer, Lawrence Levy.
Since a cut in funding in 2006, the Byre has had to abandon producing its own plays, and now provides a venue for visiting productions and community activities.