Rebuilding in 1338 instigated by the first curate, John de Crich, saw the south aisle and Chantry added.

[4] The original steeply-pitched roof was lowered in 1509, the walls over the nave arcades raised and clerestory windows inserted.

The Black Death visited Derby in 1349; a third of the population died, including sixty clergy, one of whom was the vicar of St Peter's.

Joan Waste, a St Peter's parishioner and blind rope maker, was tried for heresy at what is now Derby Cathedral in 1556.

William Cowper is said to have written, in 1768, the hymn Hark my Soul it is the Lord in the upper vestry at St Peter's.

[9] During 2010, St Peter's Church raised £6,000 to rehouse and display the Florence Nightingale stained glass window in a back-lit position at the west of the north aisle.

The window was originally commissioned in the late 1950s for the chapel at the Derbyshire Royal Infirmary, which has moved operations to Mickleover and is due for redevelopment.

In the summer of 2011, the second Derby BID (Business Improvement District) was formed with St Peter's Church at its geographical centre.

The improvements have enabled the church, as a building and a mission, to offer the St Peter's Quarter, and the city as a whole, a variety of services.