It was opened in October 1994 by Trevor Gulliver, Fergus Henderson, and Jon Spiteri on the premises of a former bacon smoke-house.

[1] Under Henderson's guidance as head chef, St. John has specialised in "nose to tail eating", with a devotion to offal and other cuts of meat rarely seen in restaurants, often reclaiming traditional British recipes.

As a result, St. John has developed a following amongst gastronomic circles: "chefs, foodies, food writers and cooks on sabbatical".

[7] The original restaurant in Smithfield was joined by a smaller, less formal sister restaurant and bakery in the Spitalfields area of London called St. John Bread and Wine in 2003,[8] and a hotel near Leicester Square in 2011.

[9] They also opened a St John restaurant in Marylebone in 2022 [10] and have three bakeries in London, in Borough Market, Covent Garden and Bermondsey.