The site was formerly Markeaton Golf Course and cost £2.5m, with a foundation stone placed on 5 July 1957 by Lord (Ernest) Hives, a former managing director of Rolls-Royce.

Opened by the Duke the day before, the 35-acre (14 ha) Bishop Lonsdale College in Mickleover was developed for teacher training courses.

At the opening ceremony, the duke said "qualities needed by teachers are the dedication of a saint, the patience of a watchmaker, the sympathy of parents, and the leadership of a general".

The Duke spent two days in Derby, staying the night nearby at Okeover Hall near Ashbourne as a guest of the Lord Lieutenant of Derbyshire.

In March 1981, the college held its first graduation ceremony with formal academic caps and gowns with only six degrees (out of 156 courses) being ratified by the CNAA.

On 4 March 1994, the B block (business and management subjects, which lies north of the East Tower) was opened by the Conservative MP, Tim Boswell.

In November 1997, the Learning Centre (now renamed ‘University Library’) was officially opened, having been built on a former car park.

In 1998, the university merged with High Peak College of Further Education in Buxton, which is in the North West of the County of Derbyshire.

High Peak College was at that time based at premises in Harpur Hill, but moved to the Devonshire Dome in the centre of Buxton in 2005.

In 2022, the university opened the Nuclear Skills Academy in partnership with Rolls Royce Submarines Ltd. with the intention of 200 new apprentices being trained for the next 10 years.

The Kedleston Road site in Allestree, in the north-west of Derby, is the largest and main campus and serves as the university's headquarters.

Derby Law School and the Department of Law, Criminology and Social Sciences operate at the One Friar Gate Square building in the centre of Derby[14] The Derby Campus also has a variety of specialist facilities, including computing laboratories, two computer games development suites, a doctor's surgery, conference facilities, multi-functional lecture theatres, art and culture venues, concert venues, recording studios, sports centre and fitness suites, outdoor pitches, student union facilities, and a multi-faith centre.

In 1854, the 6th Duke of Devonshire donated the land, part of his stables, and some of the funds for conversion to a hospital and gardens for charity patients seeking treatment at the baths in Buxton.

The ironwork dome (1881, once the world's largest, with a diameter of 44.2 metres (145 ft)), a clocktower (1882), and a surgical ward (1897) were built as expansions to the hospital, which was run by the NHS after 1948.

The University of Derby purchased the then-derelict hospital from the NHS in 2001, and moved operations here from the Harpur Hill campus in 2005.

They continue the university's training work in collaboration with Chesterfield Royal Hospital, and the building features a mock ward and 'clinical skills suite' with simulated patients to provide real-world experience for undergraduates.

The current Chancellor of the University of Derby is William Cavendish, Earl of Burlington, who was installed in a ceremony at the Buxton Campus on 15 March 2018.