The tomato leafminer, Phthorimaea absoluta (synonym Tuta absoluta Meyrick, 1917), is a transboundary plant pest that poses a serious threat to global tomato cultivation and production, with significant negative social and environmental impact from increased insecticide usage for its management. We present three P. absoluta draft mitochondrial genomes (mitogenomes) from Malawi and South Africa, thereby increasing the mitogenome resources for this invasive agricultural pest. Comparative analysis with Spain, China, and Kenya samples revealed at least seven maternal lineages across its current invasive ranges, supporting multiple introductions as a major factor for the spread of invasive populations. Mitogenome results therefore identified unexpected diversity as compared to the use of the partial mitochondrial cytochrome oxidase subunit I (mtCOI/cox1) gene marker for the inference of P. absoluta invasion biology. The whole-genome sequencing approach further identified alternative mitochondrial DNA (mtDNA) gene regions necessary to improve diversity estimates, and enables concurrent characterisation of insecticide resistance genes. Characterisation of the VSSG (Para) and AChE-1/ace-1 gene profiles that underpin pyrethroid and organophosphate (OP) resistances, respectively, confirmed co-introductions of pyrethroid and OP resistance genes into Malawian and South African populations. Our study highlights the need for additional P. absoluta mitogenome resources, especially from native populations that is needed for more accurate interpretations of introduction pathways and the development of future sustainable management strategies.