In June 1963 the Masters and Fellows of Gonville and Caius, St John’s and Trinity Colleges made known their intention to found a graduate college in Cambridge. The College was to be housed in Sir George Darwin’s home at Newnham Grange and the Old Granary.

The Founding Fellows were appointed on 1st September 1964, and consisted of Frank Hayhoe, A.C. (Bill) Stuart-Clark (Bursar), Graham Hough, Alun Moelwyn-Hughes, Abe Yoffe, Harold Whitehouse, Ronald Nedderman, Jack Goodison, John Oates, John Smart, Gerd Buchdahl and Gordon Robin.

On 28th July 1964 a Trust Deed was executed by the Senior Bursars of Trinity, St John’s and Gonville and Caius. Darwin College is founded ‘for the advancement of education, learning and research, and especially education, learning and research among graduate students and research students in the University of Cambridge’. 

The Trustees of The Rayne Foundation granted the College a sum of £500,000 payable in ten annual instalments, and the founding colleges similarly provided £160,000 over the ten years 1963-73. Max Rayne's philanthropy is commemorated by the fine portrait by Graham Sutherland, now hanging in the Hall.

In Easter Term 1965 three graduate members of the College were admitted: John Perry, Robin Carrell and Alan Cooke. By Michaelmas Term 1965 the graduate membership had grown to fourteen. In November 1965 there were 17 graduate members including Mrs Gillian Milner, the first woman member.

Architectural plans were drawn up by Architects Howell Killick Partridge and Amos for a new residential building and main entrance, linking Newnham Grange and The Hermitage, together with a dining hall adjoining The Hermitage. These plans were exhibited in 1966 at The Royal Academy Summer Exhibition.

St John’s College had indicated its willingness early on to sell The Hermitage to the new Darwin College, but it was only in 1966 that the property became vacant, when the tenant New Hall (now Murray Edwards College) moved to its permanent site and new buildings on Huntingdon Road.

The College's first Master, Frank Young, was knighted in the Queen's New Years Honours in 1973 for his contribution to biochemistry.

Her Majesty the Queen in Council on 9th June 1976 granted a Charter of Incorporation constituting the College under the name and style "The Master and Fellows of Darwin College in the University of Cambridge". With the Royal Charter were approved the first statutes of the College as a fully constituted college in the University.

In the Queen's New Year's Honours in 1979, Moses Finley received a knighthood for his contribution as Professor of Ancient History in the University. His portrait by Michael Noakes, shown here, hangs in the Dining Hall.

Cesar Milstein (1927-2002), Fellow of Darwin College, won the 1984 Nobel Prize in Physiology or Medicine for developing a technique for the production of monoclonal antibodies.

In 1986 Darwin College held a series of public lectures by eminent speakers which were well received and attended. In the second term of every academic year since then the College has organised a series of eight public lectures. Each series has been built around a single theme, approached in a multi-disciplinary way, and with each lecture prepared for a general audience by a leading authority on his or her subject.

A total of 2,830 students had pursued post-graduate studies at Darwin by 1989 when the College celebrated in its first 25 years.

Needing to house its growing student population, the College commissioned architects Dixon Jones to design a new hostel - Frank Young House - for 28 students in a leafy corner of Newnham. 

The Study Centre was opened in 1994.  Built to a design of Architects Dixon Jones, it makes the most of its narrow but sunny riverbank site, and won a RIBA design award.

Professor Geoffrey Lloyd received a knighthood in the Queen's Birthday Honours in 1997, for services 'to the history of thought’.

The Malting House on Newnham Road, a building of much architectural and historic interest, was acquired in 2002 to provide more student accommodation and guest rooms.

By 2002 the growing College community was in need of more seminar and meeting spaces. No. 1 Newnham Terrace was renovated to provide these, and a direct link into the adjacent Dining Hall was built.

As a spur to the excellent work being done by Darwin members in climate science and related fields, the College experienced its worst flooding in living memory in October 2002.

Elizabeth H. Blackburn, Darwin alumna (PhD 1975), won the Nobel Prize in Physiology or Medicine in 2009, for the discovery of how chromosomes are protected by telomeres and the enzyme telomerase.

In 2009 the College finally purchased the last of all the eight Newnham Terrace houses, meaning that all their gardens along the river were opened up for everyone to enjoy.

By 2014, when the College celebrated its 50th anniversary, a total of 7,500 students worldwide could call Darwin College their post-graduate college.

A new building and the Old Granary refurbishment were commenced in 2015 and John Bradfield Court created. Sir John Bradfield was instrumental in Darwin's foundation and remained involved until his death in 2014. 

Emeritus Fellow Richard Henderson wins the Nobel Prize for Chemistry along with Joachim Frank and Jacques Dubochet. The Nobel citation reads 'for developing cryo-electron microscopy for the high-resolution structure determination of biomolecules in solution.'

In July 2019 the Darwin College Boat Club celebrated its 50th Birthday, with a full day of events - a barbecue lunch followed by alumni and student boat races and a celebratory dinner