Field surveys over the past two decades have established that Tetranychus truncatus has become the dominant spider mite pest on major crops in China, including corn, cotton, soybean, eggplant, and cucumber. Notably, these populations exhibit a widespread infection with the endosymbiont Wolbachia. Despite its invasion into China in the late 20th century, the globally notorious Tetranychus urticae has failed to replace T. truncatus in these host plants. We sought to elucidate the molecular mechanisms underlying the dominant status of T. truncatus in China through a multi-disciplinary approach encompassing genomic evolution, population genetics, transcriptional regulation, and symbiont-host interactions. A high-quality, chromosome-level genome assembly of T. truncatus was constructed using the third-generation sequencing technology (PacBio) and Hi-C scaffolding. To analyze population structure and gene flow across China, whole-genome resequencing was performed on 343 individuals from 44 field populations. Transcriptional plasticity was evaluated through host-transfer experiments combined with comparative transcriptomic analysis to measure responses of multiply populations of T. truncatus and T. urticae when feeding on diverse plants. Furthermore, small RNA sequencing and RNAi were performed to investigate the cross-kingdom regulatory effects of Wolbachia-derived small non-coding RNAs (sncRNAs) on host reproduction. The results reveal that the expansion of gene families involved in detoxification (e.g., P450s, GSTs, UGTs) and chemosensation provides the genetic foundation for the polyphagy of T. truncatus. These gene families exhibit high levels of transcriptomic plasticity when the spider mites adapt to diverse hosts, although the overall plasticity level in T. truncatusis lower than that of T. urticae. Nevertheless, both spider mites utilize the same core detoxification enzymes to adapt to corresponding hosts, enabling rapid responses to various plant defensive stresses. Furthermore, Wolbachia-derived small non-coding RNAs (sncRNAs) were found to specifically target host mRNA, significantly enhancing the oviposition of T. truncatus and achieving symbiont-driven reproductive promotion and fitness compensation. Finally, population genomic analysis reveals prominent long-distance, cross-regional gene flow within northern T. truncatus populations, indicating that human activities may bridge geographic barriers and facilitate the rapid dispersal of resistance alleles. In conclusion, the ecological dominance of T. truncatus is orchestrated by a synergy of strong detoxification capacity, high transcriptional plasticity, symbiont-mediated reproductive gains, and human-promoted dispersal.