Wolbachia symbionts are prevalent in a wide range of arthropod and nematode hosts, and induce a variety of reproductive phenotypes that favour their spread through host populations. Among these phenotypes, parthenogenesis induction is exclusively reported in haplodiploid arthropod hosts, including spider mites and parasitoid wasps. In haplodiploids, Wolbachia manipulate the ploidy and sex determination of host embryos to generate female offspring. However, the underpinning mechanisms and the transmission mode of this remarkable phenotype remain poorly understood. In the current study, we sampled over 30 Bryobia communities and initially genotyped host and symbiont using COI and an MLST system, respectively. We subsequently formally tested the hypothesis that Wolbachia induce parthenogenesis in 4 Bryobia species (B. gigas, B. graminum, B. lagodechiana, and B. neopraetiosa) by exhaustive antibiotic treatments of virgin females that were derived from 15 isofemale lines. For all Bryobia species, we provide strong evidence that Wolbachia cause parthenogenesis. We genome-sequenced over 15 isofemale lines to further dissect this symbiosis by comparative metagenomics. We observed that a single Bryobia species exclusively carried K-group Wolbachia and was identified as B. gigas. This Bryobia species and K-group Wolbachia were the only congruent clades in our co-phylogenies, suggesting a single infection event. Remarkably, phylogenomics places K-group Wolbachia at a basal position within the large and complicated Wolbachia phylogeny. Metagenomics further reveal that K-group variants carry prophage regions, expanding our knowledge of WO bacteriophages. In contrast, B-group Wolbachia infected all other Bryobia lines and species. These B-group Wolbachia variants displayed remarkable high rates of horizontal transmission, even within species. Finally, no homology with validated genes involved in Wolbachia-mediated reproductive phenotypes was found (including parthenogenesis induction, cytoplasmic incompatibility, and male killing). Notably, the absence of insect-associated pif (parthenogenesis induction factor) Wolbachia genes suggests an independent evolution and unique mechanistic basis of this reproductive phenotype in spider mites.