Contemporary patterns of genetic variation reflect the cumulative history of a population. Population splitting, migration, and changes in population size leave genomic signals that enable their characterization. Existing methods aimed at reconstructing these features of demographic history are often restricted in their temporal resolution, leaving gaps about how basic evolutionary parameters change over time. To illustrate the prospects for extracting insights about dynamic population histories, we turn to a system that has undergone dramatic changes on both geological and contemporary timescales - an urbanized, near-shore archipelago. Using whole genome sequences, we employed both common and novel summaries of variation to infer the demographic history of three populations of endemic white-footed mice (