The introduced fungal pathogen Pseudogymnoascus destructans is causing decline of several species of bats in North America, with some even at risk of extinction or extirpation. The severity of the epidemic of white-nose syndrome caused by P. destructans has prompted investigation of the transmission and virulence of infection at multiple scales, but linking these scales is necessary to quantify the mechanisms of transmission and assess population-scale declines. We build a model connecting within-cave disease dynamics of little brown bats to regional scale dispersal, reproduction, and disease spread, including multiple plausible mechanisms of transmission. We parameterize the model using the approach of plausible parameter sets, by comparing stochastic simulation results to statistical probes from empirical data on within-cave prevalence and survival, as well as between-cave spread across a region. Our results are consistent with frequency-dependent transmission between bats, support an important role of environmental transmission, and show very little effect of dispersal among colonies on metapopulation survival. The model also offers a generalizable method to assess hypotheses about cave-to-cave transmission and to identify gaps in knowledge about key processes, and could be expanded to include additional mechanisms or bat species as research on this detrimental fungus progresses.