Environmental change reshapes species’ distributions and abundances globally, yet the numerous ways genetic variation, life-history, and climate change influence population dynamics remain poorly understood. Using 316 whole-genomes from 21 subspecies of resident and migrant song sparrows (Melospiza melodia) across western North America, we tested whether population growth was predicted by genomic offset—the mismatch between a population’s current climate-adapted genomic composition and that predicted as optimal under future or spatially distinct climates. Genomic offset explained 59% of the variation in population growth from 2001-11 to 2012-22. While genomic offsets were similar in migrant and resident populations, residents declined, especially where thermal and/or hydric stress increased, whereas migrants increased where climatic limits on population growth were ameliorated. Our results support that genomic offset can predict the dynamics of locally adapted species, highlight the potential utility of such models in conservation, and suggest seasonal migration may mitigate maladaptation to environmental change in mobile animals.