Colonial nesters are potentially susceptible to brood parasitism because they present an aggregated source of accessible nests to brood parasites. However, colonial breeding may confer fitness advantages on potential host species that outweigh the costs of parasitism, particularly if colonies are large or dense enough for corporate vigilance to deter parasitism. In addition, some studies have suggested that the spatial habitat structure near host populations is a critical determinant of parasitism rate, with cuckoos targeting those colonies close to cover. We examined the determinants of the likelihood of parasitism by Diderick Cuckoos Chrysococcyx caprius on their main southern African host, the colonially breeding Southern Red Bishop Euplectes orix, from 24 colonies and 1141 nests over two seasons. The likelihood of parasitism by Diderick Cuckoos decreased significantly with increasing colony size and nest density, but not with distance to cover from a colony, providing no support for the spatial habitat structure hypothesis. We suggest that proximate constraints, such as visibility in the semi-closed nest, limit the ability of the host to recognize the Cuckoo egg, giving rise to low rates of rejection of Cuckoo eggs. However, the Cuckoo cannot exploit this apparent weakness when the host breeding population is in large colonies that are protected by corporate vigilance. Consequently, the Diderick Cuckoo – Southern Red Bishop system may represent an evolutionary equilibrium in host and parasite defences.