Mastomys natalensis and M. coucha are commensal rodent species endemic to Africa. A recent taxonomic revision within Mastomys leaves the parasite–host list of M. natalensis questionable and that of M. coucha incomplete. The current study aimed to develop a better understanding of the ectoparasite diversity associated with the 2 distinct but closely related rodent species and to explore the influence of host and habitat type on ectoparasite infestations. Between 2014 and 2020, 590 rodents were trapped in 3 habitat types (village, agriculture and natural) across a wildlife-human/domestic animal interface. In total 48 epifaunistic species (45 ectoparasitic and 3 predatory) represented by 29 genera from 4 taxonomic groups (fleas, lice, mites and ticks) were recorded. Only 50% of the epifauna were shared between the 2 rodent species, with mites the most speciose taxon in both host species. The abundance of epifaunistic individuals, and also those of mites and fleas, were significantly higher on male M. natalensis, while ticks were significantly higher on reproductively active M. natalensis. For both rodent species, infestations by most epifaunistic taxa (on M. natalensis) and some taxa (on M. coucha) were significantly lower in the village as opposed to the less disturbed agricultural and natural habitat types. The study highlights the importance of host life history, even in closely related rodent species, in shaping parasite profiles and a loss of parasite diversity in more extreme anthropogenic habitats.