St John's has a clerestoreyed nave with N and S aisles or chapels, just two bays long and situated at the E end, in what Pevsner calls a transeptal position. The arcades are 14thc.-15thc., and they have been pierced through 12thc. walls; on the S side a 12thc. window can be seen above the arcade pier. The chancel arch is now pointed, its arch decorated with chevron, but presumably it was originally round. The figural and foliage capitals are important sculptures by the Castor workshop. There are 12thc. blind arches to either side of the chancel arch, probably, according to Pevsner, originally reredoses for side altars. The chancel has been rebuilt, perhaps in the 15thc. At the west, the tower is 14thc. in its lower parts and 15thc. above, with a crocketed spire rising behind a battlemented parapet. Romanesque sculpture is found on the chancel arch; in the corbels now in the S aisle and more re-set outside in the E wall of the S aisle; and in sections of string course set in the interior of the S aisle and the exterior E walls of both aisles.
Wakerley was held by Eudo the Steward in 1086, and a priest associated with his holding implies the presence of a church at that date. William, persona (i.e. priest) of Wakerley witnessed the foundation charter of Fineshade (founded before 1208), and R, capellanus of Wakerley, witnessed a charter referring to Laxton (also before 1208). Richard Engayne was both founder of Fineshade and the author of the charter. The first institution to be recorded was in 1220 when the advowson was in the hands of the lord of Wakerley, where it remained throughout the Middle Ages.
The church is now in the care of the Churches Conservation Trust.
Half-column responds with replaced sawtooth bases. The capitals are cushion-shaped. The N is carved with a pair of knights on horseback on the main face, leaving a castle shown on the E face and approaching a city shown on the west face. The S capital shows four monstrous creatures. On each side face is a wingless dragon with the forelegs of a lion and a long curling tail. To the right of the main face is a composite triton, perhaps best described as a representation of Capricorn. The head and forelegs are those of a goat, the torso and arms are human, and the creature has a long fish’s tail. This it holds up with its right hand, while brandishing an axe in the left. Capricorn turns to face another wingless dragon with heavy forelegs like those of a horse. A good deal of variety in surface treatment is used on these beasts; rows of beading, square lattice, sawtooth and wavy tufts of hair. Both capitals have cable neckings (two-strand on the S capital) and quirked hollow chamfered imposts. The first order arch has a fat soffit roll with angle rolls to E and W.
The order is carried on applied half columns on sawtooth bases, both original. The capitals have two-strand cable neckings and imposts continuous from the first order. The N capital is carved with a symmetrical design of Winchester acanthus. The main (S) face has a central leaf with a raised spine and veins incised to either side. The acanthus has ribbed or beaded stems and some furled leaves. The S capital has a large lion mask at the angle, with ribbed stems issuing from the mouth and terminating in a furled leaf (on the minor, west, face) and forming a loop of the main (N) face with furled leaf terminals and a flower on a side-shoot. The arch is carved with centrifugal lateral face chevron; two rolls with a pair of quirks between them and a cogwheel edge. The voussoirs towards the top of the arch are irregular and some appear to have been cut down, supporting Pevsner’s suggestion that the arch was originally round.