Dipterocarpoideae, the largest subfamily in the Meranti family (Dipterocarpaceae) are an ecologically dominant group of trees throughout much of wet tropical Asia. Increasing anthropogenic pressures on this economically important tree family make it essential to resolve their complex evolutionary relationships and understand the distribution of genetic diversity throughout the family and distribution range. Dipterocarpaceae have been the focal group in a wide range of studies, owing to their economic value, importance in historical biogeography and key role in the evolution of the Asian tropical forest biome. Despite this, persistent taxonomic and evolutionary questions remain, ranging from questions on the geographic origin, sequence of dispersal and the identification of diagnostic characters to circumscribe proper evolutionary groups. Here we present a comprehensive phylogenomic hypothesis for Dipterocarpoideae, based on the analyses of plastome and nuclear cistron (NRC) data, and provide an in-depth review on the validity of morphological characters underlying the new tribal classification proposed here for the subfamily. Phylogenomic relationships were inferred using maximum likelihood and Bayesian approaches. Estimates of origin and onset of diversification in major clades and lineages were reconstructed using plastome, nuclear and combined datasets. Results of the separate and combined genomic datasets partly corroborate elements of previous classification systems (with improved support at all levels for major clades) but provide strong support for revising the tribal classification of the subfamily into four main clades: Dipterocarpeae (Dipterocarpus), Dryobalanopseae (Dryobalanops), Shoreeae (Hopea, Neobalanocarpus, Parashorea, and all parts of a polyphyletic Shorea) and Vaterieae (including all other presently accepted Dipterocarpoideae genera). Multi-fossil-dated divergence time estimation suggests Vaterieae first originated in the Late Cretaceous, followed by Dipterocarpeae, with subsequent rise of the Dryobalanopseae and Shoreeae in the Eocene. Diversification of all tribes commenced before the Early Miocene. Our results provide strong support for the position of Neobalanocarpus heimii, Parashorea and (sub-)sections of the genera Anisoptera, Hopea, Shorea and Vatica. Hypotheses on the origin of Neobalanocarpus heimii by intergeneric hybridisation between Anthoshorea (maternally inherited) and Hopea (paternally inherited) species were corroborated. Finally, our study provides support for future revisionary changes: (1) the elevation to generic rank of sections in Shorea; and (2) revising the infrageneric classification of Hopea as all (sub-)sections were recovered as not monophyletic.