Invasive sea lamprey inhabiting the North American Laurentian Great Lakes are the target of the world’s longest running vertebrate invasive species control program. However, metapopulation dynamics comprising survival and dispersal during the sea lampreys’ lake-resident life stages are poorly understood. We applied acoustic telemetry and continuous-time multistate capture-recapture modeling to address this knowledge gap in Lake Erie. We acoustic-tagged sea lamprey (n = 619) and deployed acoustic receivers into all known connected waterways containing larval sea lamprey rearing habitat (n = 23), including the Detroit River (connecting Lake Erie to Lake Huron) and distributaries to Lake Ontario. Distribution of tagged sea lamprey to putative spawning waterways was shaped by heterogeneous stream attractiveness and distance-limited dispersal. Using parameter estimates from our capture-recapture model and simulation, we predicted survival and dispersal outcomes for a hypothetical sea lamprey population evenly distributed throughout Lake Erie at the beginning of January (34% pre-spawn mortality, 45% dispersal into Lake Erie tributaries, 19% dispersal into the Detroit River, and 2% dispersal into Lake Ontario). The methodology we applied may be widely useful for investigating dispersal and survival of aquatic organisms.