Around 1508, having inherited his father's wealth, Colet formed his plan for the re-foundation of St Paul's School, which he completed in 1512, and endowed with estates of an annual value of £122 and upwards. The school, dedicated to the Infant Jesus, was in place to give young boys a Christian education.

The celebrated grammarian william Lilye was the first master, and the company of mercers were (in 1510) appointed trustees, the first Example of non-clerical management in education. Some held Colet's religious opinions to be heretical, but william Warham, the Archbishop of Canterbury, refused to prosecute him. King Henry VIII also held him in high esteem despite his sermons against the French wars.

Colet, friend of Erasmus, had many distinguished sermons. One is the beginning of the Convocation of the clergy of Canterbury province at the London Cathedral on 6 February 1512. Archbishop Warham of Canterbury invited Colet to make the speech. Colet's speech is both direct and insightful. It represents his work, or as Colet said himself, he is "speaking out of zeal, a man sorrowing for the ruin of the Church". Furthermore, Colet stated that he came "…here today, fathers, to admonish you with all your minds to deliberate, in this your Council, concerning the reformation of the Church". The Convocation sermon is one of the most well known of his sermons. Many opinions regarding Colet, friend of Erasmus, emerged due to this sermon, in addition to the biographical information described by Erasmus. In addition, Colet gave a notable sermon before the royal court on Good Friday, 1513. He gave this speech in the wake of political tension; specifically, an English push for war against France. In his speech, Colet condemned war and prompted Christians to fight only for Jesus Christ.

Colet was rector of the guild of Jesus at St Paul's Cathedral and chaplain to Henry VIII. In 1514 he made the Canterbury pilgrimage and in 1515 preached at Wolsey's installation as cardinal.

Colet died in 1519 of the "sweating sickness." His monument was erected on the south aisle of the choir at the cathedral church of Saint Paul but destroyed in the Great Fire of London.

Colet has been studied frequently over time and has experienced resurgences in popularity. Bishop Kennett studied Colet during the seventeenth and eighteenth centuries. Kennett passed his notes to Samuel Knight who used them to write a biography of Colet which was published in 1724. During the nineteenth century, interest in Colet increased. Several editions of his works and an additional biography were published during that time. Scholars believed Colet strongly impacted his friend Erasmus and the English Reformation. Later critics went on to view Colet as Protestant-like, though historical revisionists believe that Colet was a reform preacher that wanted to improve the quality of the Church.

To this day, Colet's achievement is celebrated by St Paul's School, St Paul's Girls' School and St Paul's Juniors (formerly known as Colet Court) on John Colet Day at St Paul's Cathedral (having begun in 2003).