The theatre began life as a replacement for Aylesbury's Civic Centre Theatre. Aylesbury Vale District Council ran a public consultation on the idea in 2003, and in 2007 Norman Bragg of the London practice AedasRHWL Arts Team was commissioned to carry out the detailed design. Building work was marked by a ceremony on 24 May 2007, when Councillor Sue Polhill, then chairman of the district council, cut the first sod. Hertfordshire contractor Willmott Dixon carried out the construction.
In February 2009 Ambassador Theatre Group was named preferred management contractor for the new venue, and a six-year management agreement was signed in January 2010 by joint chief executives Howard Panter and Rosemary Squire. Aylesbury-raised actress Lynda Bellingham performed the traditional topping out ceremony on 24 April 2009 when the highest part of the structure was completed.
The opening date was announced in February 2010 and the first season went on sale that March, with Northern Ballet's Swan Lake booked as the opening performance. Cilla Black formally opened the theatre on 12 October 2010, and the launch was marked by an open air event hosted by Jonathan Wilkes and Suzanne Shaw, with guests including David Suchet, Simon Callow, Ruby Wax, Susan Hampshire and Richard O'Brien. Eric Idle sent a recorded message for the occasion.
The project was costly and much debated locally: planning permission in 2006 assumed around £25 million, the figure had reached £35 million by the time Willmott Dixon was appointed in 2008, and the final cost was £47 million. On the technical side, the acoustic design by Arup Acoustics includes a CARMEN electroacoustic enhancement system, which allows a base acoustic tuned for speech and amplified events to be made more reverberant for symphonic and choral programmes.