Invasive species are increasingly threatening ecosystems and agriculture by rapidly expanding their range and adapting to environmental and human-imposed selective pressures. The genomic mechanisms that underlie such rapid changes remain unclear, especially for agriculturally important pests. Here, we use genome-wide polymorphisms derived from native, invasive, and intercepted samples and populations of the brown marmorated stink bug (BMSB), Halyomorpha halys, to gain insights into population genomics processes that have promoted the successful global invasion of this polyphagous pest. Our analysis demonstrated that BMSB exhibits spatial structure but admixture rates are high among introduced populations, resulting in similar levels of genomic diversity across native and introduced populations. These spatial genomic patterns suggest a complex invasion scenario, potentially with multiple bridgehead events, posing a challenge for accurately assigning BMSB incursions to their source using reduced-representation genomic data. By associating allele frequencies with the invasion status of BMSB populations, we found significantly differentiated SNPs located in close proximity to genes for insecticide resistance and olfaction. Comparing variations in allele frequencies among populations for outlier SNPs suggests that BMSB invasion success has likely evolved from standing genetic variation. In addition to being a major nuisance of households, BMSB has caused significant economic losses to agriculture in recent years and continues to expand its range. Despite no record of BMSB insecticide resistance to date, our results show high capacity for potential evolution of such characters, highlighting the need for future sustainable and targeted management strategies.

allwithNZ_neutral_IQtree.phy: input file for IQtree, containing neutral SNPs of all samples and populations

allwithNZ_neutral_noNZ_BayesAss.immanc: input file for BayesAss, containing neutral SNPs of all populations except New Zealand intercepted samples

AllwithNZ_neutral_noNZ_DivMigrate.gen: input file for DivMigrate, containing neutral SNPs of all populations except New Zealand intercepted samples

AllwithNZ_noNZ_neutral_assignPOP.gen: input file for assignPOP, containing neutral SNPs of all populations except New Zealand intercepted samples

assignMC_assignPOP.R: R script for assignPOP cross-validation analysis

assignment probability plot_assignPOP.R: R script for plotting assignPOP assignment probabilities of New Zealand intercepted samples

BayesAss.sh: script to run BayesAss

BMSB_allSNPs.vcf: VCF containing all SNPs (neutral and adaptive) of all samples and populations

BMSB_BayPass.geno: genotype input file for BayPass, containing all SNPs (neutral and adaptive) of all samples and populations

BMSB_CHvsALL_BayPass.sh: script to run BayPass

BMSB_neutralSNPs.vcf: VCF containing only neutral SNPs of all samples and populations

BMSB_popmap.txt: population map of all samples and populations

ChinavsAllwithNZ_BayPass.ecotype: ecotype input file for BayPass

DivMigrate_BayesAss_heatmap.R: R script for plotting heatmaps for BayesAss and DivMigrate results

IQtree_allwithNZneutral.sh: script for running IQtree