We present the first draft genome for an invasive mite, the redlegged earth mite, Halotydeus destructor (Tucker, 1925), a major pest of Australian grains and pasture. Our de novo assembly comprised 132 contigs, with a total length of 48.90 Mb, an N50 of 874,492, an L50 of 14, a GC content of 45.3%, 14,583 putative genes, and a high level of completeness as assessed through benchmark single copy orthologs (BUSCO >89%). We use our draft genome to gain insights into the unresolved genetic mechanism of organophosphate resistance and demographic processes in the invasive Australian populations. We found that the acetylcholinesterase gene (ace), the target of organophosphate pesticides, has undergone a large amplification event in H. destructor. Copy number of this gene is considerably larger compared to most other arthropod pests and is likely to contribute to organophosphate resistance in this species. Congruent with a stepping-stone invasion pathway, we found that western populations were more genetically diverse (higher genomic heterozygosity) and had larger population sizes (as inferred from demographic analyses) relative to eastern populations. Our demographic analyses were, however, equivocal on the role of gene flow in shaping these genetic patterns. Due to the short evolutionary timescale since the H. destructor Australian invasion, it is challenging to discern between recent divergence with isolation versus ongoing gene flow. Our draft genome for H. destructor is the first assembled for mites in the family Penthaleidae of the order Trombidiformes, an under-represented group with few available reference genomes.