In addition to staging and producing entertainment, Royal & Derngate also provide a programme of creative projects in its Underground space.

[7] On the theatre's opening, The Stage newspaper reported: No element of success was wanting to contribute to the superb triumph that crowned the opening of this new theatre; the audience which thronged every available part of the house, comprised the rank and fashion of the town and county, while the charming Thespian temple, fresh from the hand of the scene painters, gleamed everywhere with light and colour.

The artistically designed scenery, the dress circle brilliant with blue and gold, the crimson rested chairs, together with the soft and delicate beauty of the ceiling and mural embellishment, were the theme of audible admiration from all parts of the house.The theatre suffered damage from fire in 1887, and was restored by Charles J. Phipps.

In the theatre's first four decades, productions of George Edwardes's musical comedies, operas, pantomimes, burlesques and melodramas were most popular.

According to director David Maloney on the DVD commentary, the theatre was chosen because it had the nearest original fly gallery to London.

Following its conception by Northampton Borough Council, RHWL designed the new theatre with Arup providing acoustic consultancy and engineering services.

[13] Most money was spent on making the theatres "more comfortable for the audiences"; new seats and air conditioning were installed, and other building systems upgraded.

The classical music season went to Spinney Hill Hall at Northampton School for Girls, while dance moved to The Castle theatre in Wellingborough.

The venue offers a diverse programme: drama, dance, stand-up comedy, classical music, children's shows, opera, and pantomime.

The venue has produced critically acclaimed shows, including Stephen Sondheim's Follies, J.B. Priestley's The Glass Cage, The Prime of Miss Jean Brodie, and Roald Dahl's James and the Giant Peach, as well as collaborating with Frantic Assembly on productions of Frankenstein and Othello.

On 16 November 2018, Jo Gordon was announced as the new chief executive of Northamptonshire Arts Management Trust and its venues, Royal & Derngate and The Core at Corby Cube.

In 2009, to celebrate its 125th anniversary, the theatres' season included a celebration of Britain's most popular living playwright, Alan Ayckbourn, a new show created with the funny company Spymonkey, and a Young America season, featuring two rarely seen plays by Eugene O’Neill and Tennessee Williams about young people in love.

In addition, Royal & Derngate played host to some of the biggest touring shows in the country, including the UK premiere of English National Ballet's Angelina Ballerina's Big Audition and Rambert Dance Company, which has returned since the redevelopment.

The Royal & Derngate host many events across the year, with touring and regional plays & musicals being some of the most popular at the box office.

Since re-opening, Royal & Derngate has worked with various writers, creative teams and companies to produce these shows, receiving considerable critical and commercial praise.

Other highlights have included the premiere of Nicholas Wright's adaptation of Pat Barker's novel Regeneration, in a co-production with Touring Consortium Theatre Company in 2014.

The programme also included a co-production of King John with Shakespeare’s Globe, and Patrick Hamilton's classic thriller Gaslight.

Shows, including 2007's 101 Dalmatians, 2018's The Worst Witch and 2019's The Season renamed Two Strangers (Carry a Cake Across New York) have gone on to be transferred to London's West End.