Phylogenetic relationships in Calochilus (∼30 species) were inferred based on a supermatrix of 81 loci including 22 species. To examine the spatio-temporal evolution of Calochilus, divergence-time estimations were conducted within a Bayesian framework using an uncorrelated relaxed molecular-clock model, followed by maximum-likelihood ancestral-range reconstructions comparing four biogeographic models. To trace the evolution of key floral and vegetative characters, maximum-likelihood ancestral-character reconstructions were carried out. The stem age of Calochilus was dated to ∼12.0 million years ago in the mid-Miocene. Divergence of Calochilus into a tropical and a temperate clade was inferred to have occurred ∼7.6 million years ago in the late Miocene. Northern Australia was reconstructed as the ancestral area of the tropical clade and the Euronotian region for the temperate clade. Range expansions from Australia to other Australasian regions, such as New Zealand and New Guinea, were inferred to have occurred only in recent geological times, commencing in the Pleistocene. The infrageneric classification for Calochilus was revised, erecting two subgenera, subgenus Calochilus and subgenus Tropichilus subgen. nov. Section Calochilus Szlach. was recircumscribed, and sect. Abrochilus sect. nov., and section Placochilus sect. nov. were erected. Identification keys to subgenera and sections and a taxonomic synopsis of the genus are provided.