The theatre opened as the New Theatre on Boxing Day 1912, designed by Richardson and Gill with Farquharson. It was renamed the New Queen's Theatre in 1915, then became the Opera House in 1920 when it passed to John Hart and his associates at United Theatres Ltd.
In 1931 it was bought by Howard and Wyndham Ltd, the company formed at the Theatre Royal, Glasgow in 1895 by Michael Simons. Under managing director A Stewart Cruikshank, and with Charles B Cochrane joining the board and working as a visiting producer, the Opera House premiered numerous musicals and revues and staged the full range of plays, opera and pantomime. It served as a cinema during the Second World War.
The theatre closed in 1979 and spent five years as a bingo hall. The Palace Trust bought it in 1984 and brought it back to life as a theatre, and Apollo Leisure took it on in 1990, filling the stage with large scale musicals. Ambassador Theatre Group acquired it in 2009, and in March 2020 the Opera House gained Charitable Incorporated Organisation status alongside the Palace Theatre. The auditorium was redecorated in March 2011, keeping its familiar green and gold scheme.
Its stage history is unusually rich. The European premiere of West Side Story took place here in 1958, and the British regional premiere of The Phantom of the Opera ran from 1993 to 1995. Gorillaz played their Demon Days Live concert here in 2005, and the theatre has since hosted a string of world premieres including Ghost The Musical, Bat Out of Hell: The Musical, The Band, & Juliet and Back to the Future: The Musical.