Over time, populations of species can expand, contract, and become isolated, creating subpopulations that can adapt to local conditions. Understanding how species adapt following these changes is of great interest, especially as the current climate crisis has caused range shifts for many species. Here, we characterize how Drosophila innubila came to inhabit and adapt to its current range: mountain forests in southwestern USA separated by large expanses of desert. Using population genomic data from more than 300 wild-caught individuals, we examine four distinct populations to determine their population history in these mountain-forests, looking for signatures of local adaptation to establish a genomic model for this spatially-distributed system with a well understood ecology. We find D. innubila spread northwards during the previous glaciation period (30-100 KYA), and has recently expanded even further (0.2-2 KYA). Surprisingly, D. innubila shows little evidence of population structure, though consistent with a recent migration, we find signatures of a population contraction following this migration, and signatures of recent local adaptation and selective sweeps in cuticle development and antifungal immunity. However, we find little support for recurrent selection in these genes suggesting recent local adaptation. In contrast, we find evidence of recurrent positive selection in the Toll-signaling system and the Toll-regulated antimicrobial peptides.