The CAP superfamily is a diverse group of proteins that are involved in different biological processes, yet their molecular functions are still incompletely understood. The α-β-α sandwich structure of the CAP domain is characteristic of this superfamily and several different domains may be found together with it. They are generally secreted proteins and in helminths many are secreted to the environment, and are related to the host-parasite interaction. In this work we mined cestode genomic data for members of this superfamily. Whereas in average 26 members with complete CAP domains were found in most cestodes, in Mesocestoides corti we strikingly found 271 members with complete domains, most of which show evidence of expression. We also found other truncated domains and putative pseudogenes. Interestingly, most of these genes were found in a monophyletic clade within a cestode-specific group of CAP domain containing proteins, and each cestode species has also developed independent duplications of these proteins. This pattern of extensive independent duplications can also be found in other parasitic and free-living flatworms, as well as in other metazoan phyla. Within the M. corti specific expansion, several sub-clades of these proteins showed evidence of evolution under positive selection. Our results suggest that the CAP domain containing proteins of animals evolve through a “birth and death” mechanism, and that different environmental pressures may drive this evolution in different species. In the case of helminth parasites, this could be related to the interaction between the parasite and the host, including mechanisms to evade and modulate the host immune system.