The firefly Photinus pyralis inhabits a wide range of latitudinal and ecological niches, with populations living from temperate to tropical habitats. Despite its broad distribution, its demographic history is unknown. In this study we modelled and inferred different demographic scenarios for North American populations of P. pyralis, which were collected from Texas to New Jersey. We used a combination of abc techniques (for multi-population/colonization analyses), and likelihood inference (dadi and StairwayPlot2, PoMo) for single-population demographic inference, which proved useful with our RAD data. We uncovered that the most ancestral North American population lays in Texas, which further colonized the Central region of the US and more recently the North Eastern coast. Our study confidently rejects a demographic scenario where the North Eastern populations colonized more southern populations until reaching Texas. To estimate the age of divergence between of P. pyralis, which provides deeper insights into the history of the entire species, we assembled a multi-locus phylogenetic data covering the genus Photinus. We uncovered that the phylogenetic node leading to P. pyralis lies at the end of the Miocene. Importantly, modelling the demographic history of North American P. pyralis serves as a null model of nucleotide diversity patterns in a widespread native insect species, which will serve in future studies for the detection of adaptation events in this firefly species, as well as a comparison for future studies of other North American insect taxa.