Founded in 1964, Darwin College was the first exclusively postgraduate college in Cambridge. Its creation was a joint undertaking by the Masters and Fellows of Gonville and Caius College, St. John's College and Trinity College, and was approved by the Council of the Senate of the University of Cambridge in June 1963. The first Master, Frank George Young, and the first twelve fellows were appointed on 5 August 1964. Initial financing of the new institution was provided by the founding colleges and the Max Rayne Foundation, with instalments received over the first ten years of the college's exstence.

The main site of the college is centered around Newnham Grange, the family home of Sir George Darwin and his wife Lady Martha "Maud" Darwin, née du Puy. At the time of their son Sir Charles Darwin's death in 1962, the property was secured by the founding colleges for the establishment of the new college, with the agreement of the family, who also agreed that the college should adopt their family name. Darwin College grew rapidly in both physical size and number of graduate students, acquiring The Hermitage, at the corner of Silver Street and Queen's Road, and the houses on Newnham Terrace. The Rayne Building was designed by Howell Killick Partridge & Amis Architects and opened in 1969. Additional buildings nearby were acquired to house the growing student body, which in 2023 numbered over 750.

Source for historical details: "Darwin College, Cambridge 1963-1973" by Frank G. Young.