A central aim of conservation is to preserve existing biodiversity and understand the ecological and evolutionary processes that support it. Inter- and intra-specific hybridization in wildlife has been recognized as a common and naturally occurring phenomenon that facilitates species adaptation and evolution. However, hybridization still constitutes one of the most challenging problems for legal protection and species management due to its perceived biological risk, lack of regulatory oversight, and different case-by-case impacts. When considering rare or threatened hybridizing species with unequal legal protection, management strategies risk being inaccurate or unsuccessful unless contextualized with an informed understanding of the species’ genetic and evolutionary backgrounds. We investigated hybridization dynamics and genetic diversity of American crocodiles (Crocodylus acutus) and Morelet’s crocodiles (Crocodylus moreletii) from Belize to ascertain whether genetic exchange through admixture displayed signs of evolutionary significance. Using genomic reduced representation (3RAD) datasets from 242 wild crocodile samples, we found evidence of population structure among C. acutus, as well as ancient bidirectional gene flow that had occurred between C. acutus and C. moreletii. Notably, we also found evidence of high levels of recent admixture along the coastal Crocodylus populations in areas with extensive habitat modification due to human impact. These findings as well as a discovered disconnect between morphological and genetic species assignments used to identify populations have implications for conservation management practices and suggest a range of additional genetic investigations to understand the natural and anthropogenic role of hybridization in large long-lived tropical predators that span marine and terrestrial ecosystems.