ABSTRACTInvasive species with native ranges spanning strong environmental gradients are well suited for examining the roles of selection and population history in rapid adaptation to new habitats, providing insight into potential evolutionary responses to climate change. The Atlantic oyster drill (Urosalpinx cinerea) is a marine snail whose native range spans the strongest coastal latitudinal temperature gradient in the world, with invasive populations established on the US Pacific coast. Here, we leverage this system using genome‐wide SNPs and environmental data to examine invasion history and identify genotype–environment associations indicative of local adaptation across the native range, and then assess evidence for allelic frequency shifts that would signal rapid adaptation within invasive populations. We demonstrate strong genetic structuring among native regions which aligns with life history expectations, identifying southern New England as the source of invasive populations. Then, we identify putatively thermally adaptive loci across the native range but find no evidence of allele frequency shifts in invasive populations that suggest rapid adaptation to new environments. Our results indicate that while these loci may underpin local thermal adaptation in their native range, selection is relaxed in invasive populations, perhaps due to complex polygenic architecture underlying thermal traits and/or standing capacity for phenotypic plasticity. Given the prolific invasion of Urosalpinx, our study suggests population success in new environments is influenced by factors other than selection on standing genetic variation that underlies local adaptation in the native range and highlights the importance of considering population history and environmental selection pressures when evaluating adaptive capacity.