Summary1. Host specificity is a major, yet poorly understood, property of parasites. Generalist parasites generally exploit a principal host species and a series of alternative host species. Understanding patterns of alternative host use may help predict phylogenetic diversification of parasite lineages and the emergence of infectious diseases. However, the ecological and evolutionary determinants underpinning alternative host use remain elusive. 2. Here, we investigated, in the wild, patterns of alternative host use in a freshwater ectoparasite copepod (Tracheliastes polycolpus), and we tested several a priori hypotheses regarding determinants underlying these patterns. We specifically answer two related questions: (i) why do parasites use alternative host species? and (ii) why do parasites preferentially use one particular alternative host species rather than another? 3. We first showed that T. polycolpus was able to use five alternative host species in addition to its principal host species, the dace (Leuciscus burdigalensis). Using causal analyses, we demonstrated that, overall, the rate of alternative host use was higher when parasite burden on the principal host was higher, providing support for the 'parasite density' hypothesis. Then, phylogenetic regressions revealed that the specific use of these alternative host species does not occur randomly, but according to the 'ecological similarity' hypothesis: parasites preferentially use host species that are ecologically close to the principal host species, irrespective of the phylogenetic distance and of the alternative host density. The fitness of parasites on alternative host species was similar to that of parasites on the principal host species, except for the smallest body-sized alternative host species for which parasite fitness was lower. Finally, using microsatellite markers, we demonstrated that this differential host use did not lead to genetically isolated parasite populations. 4. Our study suggests that encounter rate may be a key factor in predicting patterns of alternative host use and unravels intriguing questions about the contribution of phenotypic plasticity to the use of a large host spectrum by a generalist parasite.