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There are calls for research into the historical evolutionary relationships between humans and their commensals, as it would greatly inform models that predict the spread of pests and diseases under urban population expansion. The earliest civilizations emerged approximately 10 000 years ago and created conditions ideal for the establishment and spread of commensal urban pests. Commensal relations between humans and pests likely emerged with these early civilizations; however, for most species (e.g. German cockroach and black rat), these relationships have formed relatively recently-within the last 5000 years-raising the question of whether others could have emerged earlier. Following comparative whole genome analysis of bed bugs, , belonging to two genetically distinct lineages, one associated with bats and the other with humans, coupled with demographic modelling, our findings suggests that while their association with humans dates back potentially hundreds of thousands of years, a dramatic change in the effective population size of the human-associated lineage occurred approximately 13 000 years ago; a pattern not found in the bat-associated lineage. The timing and magnitude of the demographic patterns provide compelling evidence that the human-associated lineage closely tracked the demographic history of modern humans and their movement into the first cities. As such, bed bugs may represent the first urban pest insect species.