The original Denbigh School opened September 1964 where half of Wilton high's students were part of the initial intake for the school, which was located on land at the northern end of Cornwall Grove in Bletchley. In the 1980s, the Local Education Authority resolved to relocate either Denbigh or (nearby) Lord Grey School (Formerly Wilton) to Shenley Church End, a few miles to the north. Eventually Denbigh was chosen to move. In 1991-1992 term years 8 and 9 were located at the new school and other years located at the old one, the school was still in the process of being built at the time. All years moved into the new school in July 1992.
When the Shenley site opened in 1991, the site had the following areas completed, Humanities Block, Maths block 50% (Upstairs) Science Block, Technology Block, IT Room, Music Rooms, Sports hall (shared with Shenley Leisure Centre), the dining room and "the street" (an indoor communal area). Throughout that year, the English block was completed by Christmas and the playing fields by summer (prior to this the pupils in the school did outdoor PE at Loughton Middle school (Loughton County Combined School at the time) playing fields or were bussed to the Bletchley site). In 1992 the school was completed at its next phase with art rooms, an extended maths block, Modern Language block, 6th Form Block, Meeting Hall and gymnasium all opening.
Later extensions of the school involved a further extension to the art design and technology area and more recently an extended 6th form block. With the increasing popularity of IT part of the Maths block has become an ICT suite. As of July 2014, the school plans to turn its original meeting hall (opened in 1992) into a sixth form area soon after a new extension (then underway) is completed, in which there will be a new meeting hall and a new art, drama, and music department. The new extension is planned to be opened on Monday 13 April 2015.
Shortly after the move from Bletchley, the old school was demolished. However the site remained unused for some years before it was built on as an extension to the "Counties" estate in Bletchley.
In its new site, the school has delivered excellent result and is one of the leading schools in Milton Keynes in terms of academic attainment. Consequently, it has featured in the local papers from time to time because of "selection by relocation" - parents have moved home to be within its catchment area in the expectation that their child would be guaranteed entry, only to find the boundaries redrawn to cope with its permanent over-subscription for places.
As of January 2008 the school has 1440 students with 400 being in Sixth form.
The school gained specialist Technology College in 1997 under the management of Roger Connibear which entitled it to money from the Government to fund its DT facilities, computer rooms, and its further activities - such as Further Maths at A level.
The Current Headteacher is Andy Squires - who became deputy head teacher in 1997. His predecessor was Sarah Parker in 2014, who took over from Roger Connibear in 2005, who took over from Gillian Parkinson in 1993 - The latter being involved in overseeing the move to Shenley from Cornwall Grove Bletchley. In 2007 students from the school won the BBC's national Schools Question Time Competition. Students from Denbigh, and from three other winning schools, helped to produce an episode of the show, which was broadcast on 5 July 2007.
Ed Slater is an International Rugby Union player and a former pupil of Denbigh school.
Greg Rutherford is the London 2012 Long Jump Olympic Gold medalist and a former pupil of Denbigh School.
George Williams (currently at Barnsley FC) and David Moyo (recently at Northampton Town) both attended Denbigh School.