Interactions with novel environments result in both population extinctions and explosions, depending on life history strategies, ecological circumstances and historical contingencies. Understanding how populations interact with novel environments is more important now than ever because of the rapid increase in anthropogenic environmental alterations. While many native populations perish during urbanization, other populations successfully invade and thrive in these novel environments including many pests and pathogens that are detrimental to human health and economy. Pathogens contain a diversity of life history strategies and are thus good models for understanding how life history strategies interact with novel environments to promote or hinder the dynamic processes of invasion. In order to determine how life history strategies affect the evolution of a population during invasion, we studied a population of Trypanosoma cruzi – a protozoan parasite and causative agent of Chagas disease in humans – in the city of Arequipa in southern Peru. To estimate population structure and evolutionary history, we sequenced and assembled 133 T. cruzi genomes collected throughout Arequipa (N=123) and South America, and performed phylogenetic and population genetic analyses. We found that (1) the extant T. cruzi population in Arequipa was founded by a single introduction; (2) T. cruzi readily disperses between houses in a city block, but rarely disperses between blocks; (3) We resolve an apparent contradiction between the perceived clonal population structure of T. cruzi and its capacity for sexual reproduction by showing that this population regularly underwent meiosis and fertilization as the it expanded throughout the city, but that exclusive inbreeding resulted in a clonal population structure. As urbanization increases worldwide, it is important to understand how life history strategies affect the invasion of urban environments.