show Abstracthide AbstractSince Varroa destructor switched from its original host, the Eastern honeybee, to the Western honeybee, it has successfully spread worldwide and is considered the most damaging pest in beekeeping. The high inbreeding combined with bottleneck following host switch led to the assumption that V. destructor invasive populations originated from two quasi-clonal strains. Yet, Varroa mites persist after 80 years of invasion and independently develop novel traits such as acaricide resistance. How can this specialist parasite evolve new traits despite an initial loss of genetic diversity? To identify the key demographic and genetic mechanisms behind Varroa invasive success, we took advantage of our Vdes_3.0 reference genome, and a unique Varroa mite collection started in 2016. We successfully sequenced the whole genome of >1500 mites from 61 countries/islands. These samples include all known Varroa species on different hosts - and with a sampling period spanning from 1989 to 2021.