19Insect pests are characterized by expansion, preference and performance on agricultural 20 crops, high fecundity and rapid adaptation to control methods, which we collectively refer to as 21 pestiferousness. Which organismal traits and evolutionary processes facilitate certain taxa 22 becoming pests remains an outstanding question for evolutionary biologists. In order to 23 understand these features, we set out to test the relative importance of genomic properties that 24 underlie the rapid evolution of pestiferousness in the emerging pest model: the Colorado potato 25 beetle (CPB), Leptinotarsa decemlineata Say. Within the Leptinotarsa genus, only CPB has 26 risen to pest status on cultivated Solanum. Using whole genomes from ten closely related 27 Leptinotarsa species, we reconstructed a high-quality species tree of this genus. Within this 28 phylogenetic framework, we tested the relative importance of four drivers of rapid adaptation: 29 standing genetic variation, gene family expansion and contraction, transposable element 30 variation, and protein evolution. Throughout approximately 20 million years of divergence, 31 Leptinotarsa show little evidence of gene family turnover or transposable element variation 32 contributing to pest evolution. However, there is a clear pattern of pest lineages experiencing 33 greater rates of positive selection on protein coding genes, as well as retaining higher levels of 34 standing genetic variation. We also identify a suite of positively selected genes unique to the 35 Colorado potato beetle that are directly associated with pestiferousness. These genes are 36 involved in xenobiotic detoxification, chemosensation, and hormones linked with pest behavior 37 and physiology.38 39