Genus Wolbachia comprises endosymbionts infecting many arthropods and nematodes; it is a model for studying symbiosis as its members feature numerous, diverse mutualistic and parasitic adaptations to different hosts. In contrast to nematode-infecting Wolbachia, genomes of arthropod-infecting strains contain a high fraction of repetitive elements creating possibilities for multiple recombination events and causing genome rearrangements. The mechanisms and role of these features are still not fully understood. Transposons cover up to 18% of an arthropod-infecting Wolbachia genome and drive numerous genome rearrangements including inversions and segmental amplifications. ANK (ankyrin-repeat domain family) genes are also often found at the breakpoints of rearrangements, while less than 7% of them were found within locally collinear blocks (LCBs). We observed a strong correlation between the number of ANK genes and the genome size as well as significant overrepresentation of transposons adjacent to these genes. We also revealed numerous cases of integration of transposases to the ANK genes affecting the sequences and putative products of the latter. Our results uncover the role of mobile elements in the amplification and diversification of ANK genes. Evolution of arthropod-infecting Wolbachia was accompanied by diverse genome rearrangements driving the evolution of ANK genes important for bacteria-host interactions. This study demonstrates the effectiveness of our LCB-based approach to the Wolbachia genomics and provides a framework for understanding the impact of genome rearrangements on their rapid host adaptation.