For his services to the crown, Edward granted the Cantref of Dyffryn Clwyd to his close friend Reginald de Grey, baron of Wilton.

With the death of Reginald de Grey in 1308, the lordship of Ruthin passed to his son John, an important person in the history of St. Peter's.

In the year 1508 the 6th Lord de Grey of Ruthin, 3rd Earl of Kent, sold the lordship to King Henry VII.

This arrangement resulted when the originally "single rectangle" church was laterally doubled in size in the late 14th century.

The northern nave roof is particularly elaborate, with decorated beams and over 400 panels carved with an immense variety of devices, flowers, badges and heraldry of baronial families.

The later, southern roof is simpler, with plain panels but decorated bosses (and a recently painted section near the altar).

In 1589–90 Dean Gabriel Goodman purchased the church and college lands and refounded the wardenship in connection with Christ's Hospital, overseeing the construction of almshouses for twelve persons, including two women.

He had thus become the major benefactor of the town, making Ruthin a centre of ecclesiastical importance and the premier educational establishment in North Wales.

Since the demolition of the original chancel in 1663, little maintenance appears to have been undertaken to the church, as in the year 1714 a royal brief was issued to carry out urgent repairs, to the estimated value of some £3,128.

The church must have remained in a decayed condition, as during 1720/1, restoration to the stone structure, windows, timber – including a new family pew – and ironwork was undertaken at the expense of the Myddletons of Chirk Castle, who were then Lords of the Manor of Ruthin.

It appears that the work required by the brief of 1714 was not completed, as in 1754 a further brief was issued, noting that the church had "... become so ruinous and dangerous to the lives of the inhabitants".

In 1720 the Myddletons paid £28 18s 1d to the Davies brothers of Bersham, who constructed the fine wrought-iron gates of the churchyard, and in 1727 a further £20 was subscribed for their erection.

The erection of the gates enhanced the setting of the church and provided Ruthin with excellent examples of the ironsmith's craft.

Also, the standard of the Royal Air Forces Association was placed in the church "for evermore", at a service held on 29 September 1991.

Located behind St Peter's Church this attractive group of buildings give the feeling of a small cathedral close.

The Collegiate and Parochial Church of St Peter The existing stone building was erected by subscription in 1700 on the site of the original school room.