SUMMARYEnvironmental fluctuations are expected to require special adaptations only if they are associated with a decrease in fitness. We compared reproductive performance between fleas fed on alternating (preferred and non-preferred) hosts and fleas fed solely on either a preferred or a non-preferred host to determine whether (1) host alternation incurs an immediate negative effect, and, if yes, then (2) whether this effect is greater in a host specialist (Parapulex chephrenis) than in host generalists (Xenopsylla conformisandSynosternus cleopatrae). We also compared flea performance under alternating host regimes with different host order (initial feeding on either a preferred or a non-preferred host). An immediate negative effect of alternating hosts on reproductive performance was found inP. chephrenisonly. These fleas produced 44·3% less eggs that were 3·6% smaller when they fed on alternating hosts as compared with a preferred host. In contrast,X. conformisandS. cleopatraeappeared to be able to adapt their reproductive strategy to host alternation by producing higher quality offspring (on average, 3·1% faster development and 2·1% larger size) without compromising offspring number. However, the former produced eggs that were slightly, albeit significantly, smaller when it fed on alternating hosts as compared with a preferred host. Moreover, host order affected reproductive performance in host generalists (e.g. 2·8% larger eggs when the first feeding was performed on a non-preferred host), but not in a host specialist. We conclude that immediate effects of environmental fluctuation on parasite fitness depend on the degree of host specialization.