Classic invasion biology theory posed that invasions stem from introductions of few individuals that create a limited pool of genetic and phenotypic diversity for future adaptation. However, a rising number of examples highlight high levels of genetic diversity, extensive admixture, and the potential for rapid adaptation following introduction. The worldwide introduction of white clover, Trifolium repens L., to multiple different regions during the 1700’s and subsequent establishment and spread presents a unique opportunity to examine the role of rapid adaptation in invasions. Here I leverage a transcontinental provenance study conducted in the native and introduced ranges of white clover as well as a large worldwide population genomics dataset to determine the extent and costs of adaptation following introduction as well as regions of the genome underlying adaptation. Introduced populations show distinct signatures of local adaptation to novel conditions within the introduced range. However, there is a clear cost to adaptation as introduced population have lower fitness in native populations with similar abiotic climates. Native and introduced populations form nearly entirely non-overlapping clusters in PCA analysis stemming from distinct introduction histories, introgression with cultivars, as well as adaptation. Population genomic outlier analysis between native and introduced populations suggest that many genomics regions show signatures of selection. While many more of these regions are shared between different introductions than expected by chance, few regions are shared across all introductions. We focus on one key candidate region of the genome containing a putative inversion that segregates at relatively high frequency in North and South America, but that is at low frequency within the native range. This region co-locates to a large-effect fitness QTL within common garden sites in the introduced range suggesting that this locus may underlie adaptation to novel environments during invasion. Together, our results emphasize the complex and intertwined roles that colonization history, introgression and selection play in adaptation to novel environments during an ongoing invasion.