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Introduction: Host shifts of parasites can have devastating effects on novel hosts. One remarkable example is that of the ectoparasitic mite Varroa destructor, which has shifted hosts from Eastern honey bees (Apis cerana) to Western honey bees (Apis mellifera) and posed a major global threat to apiculture and wild honey bees. Objectives and methods: To uncover the mechanisms underlying this rare successful host shift, we conducted a whole-genome analysis of host-shifted and nonshifted V. destructor mites and a crossfostering infestation experiment. Results: We found that oogenesis was upregulated in host-shifted mites on the new host A. mellifera relative to nonshifted mites. The transcriptomes of the host-shifted and nonshifted mites significantly differed as early as 1 h post-infestation of the new hosts. The differentially expressed genes were associated with nine genes carrying nonsynonymous high-FST SNPs, including mGluR2-like, Lamb2-like and Vitellogenin 6-like, which were also differentially expressed, and eIF4G, CG5800, Dap160 and Sas10, which were located in the center of the networks regulating the differentially expressed genes based on protein– protein interaction analysis. Conclusions: The annotated functions of these genes were all associated with oogenesis. These genes appear to be the key genetic determinants of the oogenesis of host-shifted mites on the new host. Further study of these candidate genes will help elucidate the key mechanism underlying the success of host shifts of V. destructor.