Abbot Hugh of Eversden began to rebuild this ruined part of the church, and this accounts for the five bays of the nave arcading westward of the rood-screen being in fourteenth-century style. He did not live to finish all this work, but it was carried on by his successor, Richard of Wallingford (1326-1335), and finished by the next Abbot, Michael of Mentmore, about 1345. The present rood-screen, which probably took the place of a previously existing one of Norman date, was built in 1360 by Thomas de la Mare. No further change of importance was made until the time of John of Wheathampstead, who was Abbot from 1420 to 1440, and again from 1451 to 1464. He left his marks in various parts of the Abbey, and for the most part his work was bad: he did almost as much to injure the Abbey as the nineteenth-century restorers who swept away much of his work have done. He rebuilt all the upper part of the west front, and inserted Perpendicular windows at each end of the transept; he turned the high-pitched roofs of nave and transepts into flat ones, and lowered the slope of the roofs of the aisles. His object in doing this was to be able to use the old beams again whose ends were decayed, and which were shortened by cutting off the unsound parts. The result of this was that the Norman triforium arches on the north side were thrown open to the sky; these he filled with Perpendicular tracery, converting them into windows. The tracery still remains, although the new roof has the same slope as the original one, and the triforium is now again inclosed beneath it. He also pulled down the wooden octagon on the central tower. His chantry on the south side of the high altar was probably erected soon after his death.
Abbot William of Wallingford (1476-1484) built the high altar screen, carrying out a plan which John of Wheathampstead had not been able to accomplish. The only addition made after this to the Abbey is the chantry of Thomas Ramryge, who became Abbot in 1492. The exact date of its construction is not known, all records of the Abbey during Ramryge's rule having perished; but from its style it is generally supposed to have been built about the year 1520. During the reign of Henry VIII. all the monasteries were dissolved; first the smaller, then the more important ones, among them that of St. Albans. The fortieth and last Abbot of St. Albans, Richard Boreman of Stevenage, surrendered the Abbey on December 5th, 1539, he and the monks receiving pensions as compensation.
In February of the following year the King granted to Sir Richard Lee all the monastic buildings, but not the Abbey Church or the adjoining Chapel of St. Andrew, with all the land lying round the Abbey Church. Lee promptly proceeded to destroy all the domestic buildings. The church remained in the possession of the Crown till 1553, when the town obtained a charter from Edward VI. This, among other provisions, empowered it to erect a grammar school within the church or in some other convenient place. The town authorities thereupon converted the Lady Chapel and the retro-choir into the grammar school. A passage was cut through the retro-choir, bounded by brick walls on either side; this was used as a public pathway until 1874, when it was closed, and again became part of the church. The part to the east of the passage served as the grammar school until 1870. The mayor and burgesses by the same charter received the Abbey Church, in return for £400, to be used as their parish church; and in May, 1553, the first rector, George Wetherall, took charge of the building.
The parishioners thus found themselves in possession of an enormous building which they had not sufficient money to keep in proper repair. In 1612, and again in 1681, briefs or letters patent were issued by royal authority, ordering collections to be made in all churches in England for the repair of St. Albans Church. In 1689 a grant was made by William and Mary. These sums were spent on various repairs, such as altering the belfry windows, "filling up" with earth "the hollow in the wing," that is, raising the level of the floor of the south arm of the transept. In 1695 similar work was done in the north aisle; in 1704 a new window, a wooden one, was inserted in the south end of the transept, in place of Wheathampstead's, which had been blown in by a gale during the previous year. There are records of £100 being spent in recasting some of the bells between 1705 and 1707.
Money was again collected in 1721 by letters patent, and this was spent on repairing the ceilings. About the same time a legacy was spent in repaving the nave, and the west ends of the aisles were blocked by brick walls. Some slight repairs were done about 1764, when a fresh collection was made.
More extensive repairs were made in 1832: the roof was releaded, such of the clerestory windows as had been closed were reglazed, and the south window of the transept was rebuilt in stone. The choir, after the repairs, was opened for service in 1833. The nave to the west of the rood-screen was more or less in a dilapidated condition, protected by the releaded roof, but not used. The presbytery had been fitted up in Georgian style as a chancel, the organ stood in the north arm of the transept, and high pews filled the choir westward as far as the rood-screen. This was the condition of the part of the church which was used up to 1870.