In 1423 Richard "Dick" Whittington, the fabled Lord Mayor of London, was buried within its precincts; although the tomb is now lost.

The suffix Royal is first recorded in the next century and refers to another nearby street, now vanished, called Le Ryole, which was a corruption of La Reole, a town in Bordeaux.

One of his earlier philanthropic acts, made in 1409, was to pay for the rebuilding and extension of St Michael Paternoster Royal after a vacant plot of land was acquired in Le Ryole.

John Stow records that Whittington's body was dug up by the then Rector Thomas Mountain, during the reign of Edward VI, in the belief that he had been buried with treasure.

Other worthies buried in the pre-Fire church were William Oldhall (d. 1459) Speaker of the House of Commons, the Lord Mayors John Yonge (d. 1466) and William Bayley (d. 1524), Peter Blundell (d. 1601) founder of Blundell's School, (mentioned in Blackmore's novel Lorna Doone) and the Cavalier poet John Cleveland (d. 1658).

Building began again the next year, supervised and built by Wren's master mason Edward Strong the Elder.

St Michael's underwent a number of renovations in the 19th century, by James Elmes in 1820, William Butterfield in 1866 and Ewan Christian in 1894.

A proposal by the diocese to demolish the walls and preserve the tower only was successfully opposed by the City of London Corporation, and the church restored by Elidir Davies between 1966 and 1968.

[12] In 2024, it was put up for sale[13] and was described in the marketing material as a “former Wren church” and "Benefits from three floors of open plan offices".

Following bomb damage, these buildings were cleared and Whittington Garden laid out on their site, so that St Michael's main façade is now on the south, along Upper Thames Street.

The height of the tower and steeple is 128 ft. St Michael Paternoster Royal was designated a Grade I listed building on 4 January 1950.

The west of the building, roughly corresponding with the plan to the original 13th-century church, accommodates a hall, vestibule and the offices of the Mission to Seafarers.

The windows on either side show the Virgin Mary with the infant Jesus[16] and Adam and Eve with St Gabriel and the serpent.

Before it are seventeenth-century Baroque statues of Moses and Aaron, moved here from All-Hallows-the-Great on that church's demolition in 1894: the statues’ hands were blown off in the war and have been replaced; Moses previously held a pointer, indicating the Decalogue, while Aaron held a censer – he now raises his hands in a blessing.