In a globalized world, parasites are often brought in contact with new potential hosts. When parasites successfully shift host,
severe diseases can emerge at a large cost to society. However, the evolutionary processes leading to successful shifts are
rarely understood, hindering risk assessment, prevention, or mitigation of their effects. Here, we screened populations of
Varroa destructor, an ectoparasitic mite of the honeybee genus Apis, to investigate their genetic structure and reproductive
potential on new and original hosts. From the patterns identified, we deduce the factors that influenced the macro- and microevolutionary
processes that led to the structure observed. Among the mite variants identified, we found two genetically similar
populations that differed in their reproductive abilities and thus in their host specificity. These lineages could interbreed,
which represents a threat due to the possible increased virulence of the parasite on its original host. However, interbreeding
was unidirectional from the host-shifted to the nonshifted native mites and could thus lead to speciation of the former. The
results improve our understanding of the processes affecting the population structure and evolution of this economically
important mite genus and suggest that introgression between shifted and nonshifted lineages may endanger the original host.