Simple SummaryIn this study, we produced a genomic resource for the light brown apple moth, Epiphyas postvittana, to understand the biological basis of adaptation to a high number of hosts (polyphagy) and the invasive nature of this and other lepidopteran pests. The light brown apple moth is an invasive pest of horticultural plants, with over 500 recorded plant hosts. With origins in Australia, the pest has subsequently spread to New Zealand, Hawaii, California and Europe, causing significant economic losses for fruit producers. Comparative genomic analyses with other lepidopteran genomes indicate that a high proportion of the genome is made up of repetitive sequences, with the majority of the known elements being DNA transposable elements and retrotransposons. Twenty gene families show significant expansions, including some likely to have a role in its pest status. Finally, population genomics, investigated by a RAD-tag approach, indicated likely patterns of invasion and admixture, with Californian moths most probably being derived from Australia.The light brown apple moth, Epiphyas postvittana is an invasive, polyphagous pest of horticultural systems around the world. With origins in Australia, the pest has subsequently spread to New Zealand, Hawaii, California and Europe, where it has been found on over 500 plants, including many horticultural crops. We have produced a genomic resource, to understand the biological basis of the polyphagous and invasive nature of this and other lepidopteran pests. The assembled genome sequence encompassed 598 Mb and has an N50 of 301.17 kb, with a BUSCO completion rate of 97.9%. Epiphyas postvittana has 34% of its assembled genome represented as repetitive sequences, with the majority of the known elements made up of longer DNA transposable elements (14.07 Mb) and retrotransposons (LINE 17.83 Mb). Of the 31,389 predicted genes, 28,714 (91.5%) were assigned to 11,438 orthogroups across the Lepidoptera, of which 945 were specific to E. postvittana. Twenty gene families showed significant expansions in E. postvittana, including some likely to have a role in its pest status, such as cytochrome p450s, glutathione-S-transferases and UDP-glucuronosyltransferases. Finally, using a RAD-tag approach, we investigated the population genomics of this pest, looking at its likely patterns of invasion.