As species respond to changing climate, distributions and abundances may shift and alter species interactions. Hybridization, a relatively widespread phenomenon becoming more common with climate change, can have detrimental effects on population growth rates and genetic integrity. Beneficial effects due to the introduction of advantageous alleles and increased genetic diversity may result from hybridization as well. Species may also accrue fitness costs associated with changing climates if mismatches occur between environmental variables and phenotypes. The gray-headed chickadee, Poecile cinctus lathami, is an extremely rare songbird that has experienced marked declines in recent decades within its restricted distribution in Alaska and northwestern Canada. The widespread boreal chickadee, Poecile hudsonicus, has conversely become more locally abundant. We investigated two hypotheses of mechanisms – hybridization and environmental change – that may have contributed to the apparent rapid decline of the gray-headed chickadee and influx of boreal chickadee using mitochondrial and reduced representation nuclear DNA sequence data. We analyze historical specimens of both species and contemporary boreal chickadees to investigate the occurrence of hybridization and trends of abundance and interspecific gene flow. We also test for gene-environment associations using historical, present, and future climate data sets to explore the trajectory of boreal chickadee adaptation to their local environment. We detect evidence of hybrids backcrossing to boreal chickadee populations prior to recent declines, and signatures of later-generation hybrids among both historical and contemporary boreal chickadees. We find that boreal chickadee genetic isolation-by-environment exceeds isolation-by-distance. Further, we identify temperature and precipitation bioclimatic variables which have strong associations with allelic composition, and predict areas with the highest risk of environmental-genetic mismatch due to climate change. This study identifies hybridization as playing a role in gray-headed chickadee declines despite the inability to sample any individuals today, and provides evidence that environment-genetic mismatches may occur for boreal chickadees as a result of climate change across areas of sympatry and allopatry.