The Tunstal Chapel is the larger of the castle's two chapels and was built by Bishop Tunstal in the 1540's at the same time as the Tunstal Gallery. Originally the chapel was shorter, the original line of the altar being shown by the position of the piscina hidden behind the wall panelling on the right-hand side. The chapel was extended by Bishop Cosin and Bishop Crewe in the late seventeenth Century and the extension is obvious from the pronounced change in stonework between the east and west ends. The stonework of the east window is the original, having been moved when the extension was built, and the stained glass dates from the late nineteenth century.

Some of the seats towards the back of the chapel are sixteenth century 'misericords' (meaning 'mercy seats'), which were designed to be lifted up so that a person standing for long periods of time could rest on the ledge on the underside of the seat. The decorative organ pipes (which hide a modern organ) and the woodwork beneath are seventeenth century and come originally from Durham Cathedral, which is just a few hundred yards away. The altar and reredos (the screen behind the altar) date from the late nineteenth century, although the central carvings were originally part of seventeenth century German pulpit.

Having been built around 1078, the Norman Chapel is the oldest part of the castle readily visitable. The style of the architecture is remarkably Saxon, especially the deep groin vaulting in the ceiling, close pillars and herringbone floor, and may be due to forced Saxon labour after the Norman invasion.

The room was scarcely used only some fifty years after its completion, and by the fifteenth century was inaccessible and deprived of light - enlargement of the keep mound blocking off the three original windows of the east wall. Left for some hundreds of years the chapel was finally re-entered in the late eighteenth century, but was ignored. In 1841 it was decided to use the room as a corridor up to the keep, newly rebuilt for student rooms, and the present entrance and part of the far wall were knocked through. The use of the chapel changed again during the Second World War when it became an RAF observation / command post. With the room better lit, the ceiling and carvings were more clearly visible, and the remarkable nature of the room was recognised. Consequently, after the war, the east wall was resealed and the room was consecrated for use as the castle's second chapel, thereby returning the chapel to its original use.

The organ originates from the Father Smith instrument in the Cathedral, built in 1667. In 1873 the Smith organ, by this time on the floor east of the choir stalls in the Cathedral Choir, was dismantled. Most was stored and ultimately the pipework and working parts lost, but the Chair organ was acquired and installed by Harrison & Harrison on the west gallery behind the old Smith Chair case in the Tunstall Chapel. The overal structure, three stop Great, Pedal, and action were all new, but the previous Cathedral Chair organ formed a Swell division in a new box.

In 1925 Harrison & Harrison rebuilt the instrument in its "multum in parvo" style, with standard console and fittings. The organ was refurbished and the specification was changed again, to that found today, by Brian Brighton on behalf of J.W.Walker in 1981, with the pipework for the Fifteenth and Octave Geigen derived from the previous Contra Dulciana and Salicional respectively.

Further refurbishment work has been undertaken in 2005.