Mitochondrial introgression between species plays an important role in shaping the reproductive isolation, genetic diversity, and physiology of animals, including arthropods. Yet, the ecological and evolutionary factors that promote initial interspecific introgression and subsequent spread of introgressed haplotypes remain poorly understood. In the cosmopolitan spider mite genus Tetranychus, divergent mitochondrial lineages segregate within populations and species. Here, we unravel the cryptic mtDNA diversity of seven sympatric and allopatric Tetranychus species by leveraging complete circular mitochondrial genomes with COI markers. Using a combination of long-read and short-read genotyping across more than 100 isogenic lines, we identified multiple independent and ongoing introgression events that generate deep incongruences between nuclear and mitochondrial phylogenies. We subsequently tested whether maternally transmitted symbionts shape the spread and distribution of mitochondrial haplotypes within and between Tetranychus species. Using unbiased and targeted genetic approaches, we genotyped our reference panel for all potential symbiont infections. We detected substantial variation in infection frequencies across mitochondrial lineages for several bacterial symbionts. We further tested the role of the evolution of mitochondrially encoded pesticide resistance in facilitating these introgression events. By combining toxicity assays with a systematic identification of target- site mutations, we assess if particular haplotypes confer selective advantages under agricultural pesticide exposure, providing a mechanistic link between mitochondrial variation, adaptive responses, and interspecific hybridization in pest populations. Finally, we also confirm that ecological factors, such as host plant use and geographic distribution, do not play a major role in mitochondrial introgression across species boundaries. Together, our findings highlight how both natural and agricultural pressures may drive the spread of particular mtDNA haplotypes, demonstrating how interspecific introgression may facilitate rapid adaptive responses in important mite pest species.