Despite a growing appreciation for the generative role hybridization can play in adaptive radiation, we do not know how extensively radiating lineages differ from their non-radiating counterparts in their history and capacity for hybridizing. My research leverages a rare and young radiation of Caribbean pupfishes that occurs only on a single island, yet is nested within a large network of single species lineages on similar islands, to test out hypotheses against. Using the genomes of 250 pupfish from across Cyprinodon’s range, I characterized the distribution of genetic variation across the Caribbean. Despite constraint to a single island, most of the genetic variation involved in the radiation is widespread across Caribbean populations. Some was even brought in through hybridization and introgression may have modified the fitness landscape and increased craniofacial trait diversity. The radiation contains stronger signatures of adaptive introgression than found in populations on other islands that did not radiate, lending support to the hybrid origins hypothesis. However, these other populations did experience introgression from some of the same sources and in some cases share 100% of the same genetic variation, highlighting that there is still much to learn about why introgressed variation aids adaptive radiation in only certain cases.