Parallel evolution can occur through novel mutations, standing genetic variation, or adaptive introgression. Uncovering parallelism and introgressed populations can complicate management of threatened species, particularly as admixed populations are not generally considered under conservation legislations. We examined high coverage whole-genome sequences of 30 caribou (Rangifer tarandus) from across North America and Greenland, representing divergent intra-specific lineages, to investigate parallelism and levels of introgression contributing to the formation of ecotypes. Caribou are split into four subspecies and 11 extant conservation units, known as Designatable Units (DUs), in Canada. Using genomes from all four subspecies and six DUs, we undertake demographic reconstruction and confirm two previously inferred instances of parallel evolution in the woodland subspecies and uncover an additional instance of parallelism of the eastern migratory ecotype. Detailed investigations reveal introgression in the woodland subspecies, with introgressed regions found spread throughout the genomes encompassing both neutral and functional sites. Our comprehensive investigations using whole genomes highlight the difficulties in unequivocally demonstrating parallelism through adaptive introgression in non-model species with complex demographic histories, with standing variation and introgression both potentially involved. Additionally, the impact of parallelism and introgression on the designation of conservation units has not been widely considered, and the caribou designations will need amending in light of our results. Uncovering and decoupling parallelism and differential patterns of introgression will become prevalent with the availability of comprehensive genomic data from non-model species, and we highlight the need to incorporate this into conservation unit designations.