- We studied survival and development of preimagoes and the ability to withstand starvation of adults in two flea species, host‐specific Parapulex chephrenis and host‐opportunistic Xenopsylla ramesis, when parent fleas fed on a typical (Acomys cahirinus and Dipodillus dasyurus, respectively) or an atypical (D. dasyurus and A. cahirinus, respectively) rodent host that either had never been parasitized by fleas (pristine) or had previously been exposed to fleas. We asked whether a repeatedly infested host acquired resistance that would cause decreased viability of the next generation fleas. Survival of preimaginal P. chephrenis was similar, independent of host species or its infestation status. Preimaginal X. ramesis had a higher survival rate when their parents fed on preinfested than on pristine typical hosts, whereas no effect of infestation status of an atypical host was found. P. chephrenis developed faster if their parents fed on atypical than on typical hosts and on pristine than on preinfested hosts of either species. X. ramesis developed faster if parents fed on pristine than preinfested typical hosts, but no difference in duration of development was found for atypical hosts. Under starvation, P. chephrenis lived longer if their parents fed on preinfested than on pristine typical hosts, but their lifespan did not depend on infestation status of atypical hosts. The latter was also true for X. ramesis and both host species. We conclude that a host is constrained in its ability to cope with a parasite, whereas a parasite is able to cope with defence responses of a host. J. Exp. Zool. 313A:680–689, 2010. © 2010 Wiley‐Liss, Inc.