Founded as a chantry school, it fell foul of the Protestant reformers and was only saved from destruction under the Chantries Act of Edward VI by the personal intervention of Sir William Cecil (later Lord Burghley) who worked in the service of Edward Seymour, 1st Duke of Somerset and who secured a specific Act of Parliament in 1548 ensuring its survival.

This building continued in use as a school room until the early twentieth century when it was restored and extended and, in 1930, returned to use as a chapel.

In 1961, a nineteenth-century Gray and Davison pipe organ was installed[2] although this was removed in the 1990s and replaced with an electronic substitute.

Over its history the school has built or absorbed seventeenth-, eighteenth- and nineteenth-century buildings, besides the site of a further demolished medieval church (Holy Trinity/St Stephen's) and remains of Brazenose College built by the secessionists from the University of Oxford in the fourteenth century.

Both Stamford Town Council and St John's College still have nominees on the school's governing body.

This trust had been established for the relief of poverty by William Browne (died 1489), another wealthy wool merchant and alderman of the town, and his gift is commemorated in the name of a school house.

This local form of the Assisted Places Scheme provided funding to send children to the two schools that were formerly direct-grant grammars.