The Betta fish displays a remarkable variety of phenotypes selected during domestication. However, the genetic basis underlying these traits remains largely unexplored. Here, we report a high-quality genome assembly and resequencing of 727 individuals representing diverse morphotypes of the Betta fish. We show that current breeds have a complex domestication history with extensive introgression with wild species. Using a genome-wide association study, we identify the genetic basis of multiple traits, including coloration patterns, the “Dumbo” phenotype with pectoral fin outgrowth, extraordinary enlargement of body size that we map to a major locus on chromosome 8, the sex determination locus that we map to dmrt1 , and the long-fin phenotype that maps to the locus containing kcnj15 . We also identify a polygenic signal related to aggression, involving multiple neural system-related genes such as esyt2 , apbb2 , and pank2 . Our study provides a resource for developing the Betta fish as a genetic model for morphological and behavioral research in vertebrates.