On graduation with degrees in both Architecture (1951), when he was awarded the RIBA President’s Honorary Silver Medal, and Town Planning (1952), Bonnington took up a town planning appointment in Memphis Tennessee. This gave him an opportunity to travel throughout the USA and visit the work of Frank Lloyd Wright and Mies Van Der Rohe, experiences that influenced much of his later work.

On returning to the UK and after serving for two years with the Royal Engineers he joined the newly formed studio of Sir Basil Spence in Canonbury Place, North London, working on the design and construction of Coventry Cathedral. In the early 1960s and following the completion of the Cathedral, he proceeded to work on the masterplans and major faculty buildings for Southampton, Sussex and Exeter Universities.

In 1963 Sir Basil Spence restructured his practice into three separate partnerships practicing as Sir Basil Spence OM RA from his Canonbury office, Sir Basil Spence, Glover and Ferguson in Edinburgh and Sir Basil Spence, Bonnington & Collins operating from 1 Fitzroy Square London.

In this form, the partnership became one of the first multi-disciplinary integrated design offices in the UK, with planners, landscape designers, architects, interior and furniture designers, mechanical services engineers and cost consultants working together in a studio environment.

At this time Jack designed and built Ferrum House in Hertfordshire which featured in the “House and Garden Book of Modern Houses” was subsequently Listed Grade II and featured in the Twentieth Century Society compilation of The Best 100 Houses.

During the 60s and 70s in addition to the numerous faculty buildings completed at the Universities of Exeter, Sussex and Southampton, the firm’s work included the British Pavilion at Expo 67 Montreal, Salter’s Hall in the City of London, Hampstead Civic Centre, Kensington and Chelsea Town Hall, Westminster Tower on the South Bank and Sunderland Civic Centre.

In 1973 the practice reformed as the John S. Bonnington Partnership moving that same year from its Fitzroy Square office in London to the refurbished Grade I Listed Tyttenhanger House in Hertfordshire. This introduced the practice to the care and refurbishment of heritage buildings such as Salisbury Hall in Hertfordshire and subsequently overseas.

International success saw the Bonnington’s practice take up projects in Paris, Cyprus, the Middle East, Singapore, Malaysia, Hong Kong, China, Australia, Guam, Hawaii and most significantly in Japan.

Many of the partnership’s buildings, designed under Jack's leadership, were award winners and Listed by Historic England, including six faculty buildings at Sussex University, the Swiss Cottage Library, Salter’s Hall and his own house in Hertfordshire.