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In the early 1990s, as the Human Genome Project was getting under way, the former Nuffield Professor of Medicine, John Bell (now Regius Professor Sir John Bell), successfully applied for support from the Wellcome Trust to establish the Centre. It opened in 1994, one of the first of a cluster of new biomedical research laboratories to be established on the Churchill Hospital site in Headington. Professor Bell recruited Mark Lathrop from the pioneering Centre d’Études de Polymorphisme Humaine in Paris as its co-founder and scientific director.

On Professor Lathrop’s return to Paris in 1998, the neurogeneticist Professor Anthony Monaco took over, expanding research on the biological basis of disease and doubling the size of the centre’s staff. The Centre moved to its own purpose-built £27m premises, the Henry Wellcome Building of Genomic Medicine, in 1999.

Professor Peter Donnelly was Director of the centre from 2007 - 2018.  Under his leadership the laboratory was extended to accommodate the continued expansion of the Centre’s research effort. In 2010 Professor Yvonne Jones, joint head of the Structural Biology Division (STRUBI), became Deputy Director of WCHG. In 2019 John Todd, Professor of Precision Medicine and Director of the Diabetes and Inflammation Laboratory was appointed Director of the WHG and Julian Knight became Deputy Director.