Many highly recognisable species lack genetic data important for conservation due to neglect over their hyperabundance. This likely applies to the Sulphur-crested Cockatoo (Cacatua galerita), one of the world’s most iconic parrots. The species is native to Australia, New Guinea and some surrounding Melanesian islands. Four subspecies are currently recognised based on morphology. Australian subspecies and populations are abundant, but several factors threaten those in New Guinea and Melanesia. Genetic data from natural populations are scarce – information that is vital to identifying evolutionarily significant units (ESUs) important for modern conservation planning. We used whole-genome resequencing to investigate patterns of differentiation, evolutionary affinities and demographic history across C. galerita’s range to assess whether currently recognised subspecies represent ESUs. We complement this with an assessment of bioacoustic variation across the species’ distribution range. Our results point to C. galerita sensu lato (s.l.) comprising two species. We restrict C. galerita sensu stricto (s.s.) to populations in Australia and the Trans-Fly ecodomain of southern New Guinea. The second species, recognised here as Cacatua triton, likely occurs over much of the rest of New Guinea. Restricting further discussion of intraspecific diversity in C. triton, we show that within C. galerita s.s. two ESUs exist, which align to Cacatua galerita galerita in eastern Australia and southern New Guinea and Cacatua galerita fitzroyi in northern and north-western Australia. We suggest that the evolution of these species and ESUs are linked to Middle and Late Pleistocene glacial cycles and their effects on sea level and preferential habitats. We argue that conservation assessments need updating, protection of preferential forest and woodland habitats are important and reintroductions require careful management to avoid possible negative hybridization effects of non-complementary lineages.