Admixture is an evolutionary process that enables short-term adaptation. The Creole cattle from Guadeloupe is a tropically adapted breed. Its three-way admixture and long-term isolation offer a unique opportunity for understanding the genetic determinants of adaptive admixture in livestock. Here, we sequenced 23 Creole cattle from Guadeloupe (GUA) and combined our data with sequenced genomes of 99 cattle from 25 breeds representative of European, African and indicine groups to provide the most detailed exploration, to date, of patterns of genetic variation and to detect selection signatures in this population. We detect 17 228 983 single nucleotide polymorphisms (SNPs) and we confirmed the higher level of African and indicine ancestries, compared to the European ancestry, in the GUA genome. We show that, unlike Criollo cattle, GUA population originates directly from West Africa with indicine ancestry inherited via West African ancestors. We relied on consistency of signals across various methods based on excess of haplotype homozygosity, differences in allele frequencies and excess ⁄ deficiency of local ancestry to identify five strong candidate regions showing an excess of indicine ancestry. These encompass immune-, heat-tolerance- and physical exercise-related genes. Moreover, we found that a previously identified horn-related gene, RXFP2 is under strong selective pressure in GUA genome likely owing to human-driven (socio-cultural) pressure. Our study highlights the role played by population admixture for driving rapid adaptive response to local environmental constraints.