Pantropical taxa with broad and changing distributions provide useful systems for assessing drivers of tropical tree biodiversity. Xylopia, a vertebrate-dispersed woody plant genus with species evenly distributed across the tropics, including on isolated islands, occurs in rainforest as well as in subhumid, inundated, and ultramafic habitats. To determine the significance of biogeographic and ecological transitions in the genus, we generated reconstructions for 168 species using a nuclear phylogenomic framework. Xylopia originated at the Eocene-Oligocene boundary with the ancestral area reconstructed as paleotropical. A core clade, comprising 90% of species, dispersed once from Africa to the Asia-Pacific area and once to the Americas. Five lineages dispersed between Africa and Madagascar; in the Asia-Pacific area, multiple dispersals occurred between the Sunda and Sahul plates. Niche conservatism in continental rainforests continued, while the genus repeatedly dispersed, overcoming environmental filters to occupy novel environments. Notably, diversification continued in drier subhumid environments as many rainforest groups underwent extinction, and species richness on islands showed no correlation with isolation index. Novel environments largely acted as sinks, together encompassing about half the species in the genus. High value seed rewards taken by birds that transit long distances, combined with the capacity to transition to novel habitats, were fundamental drivers of pantropical expansion and diversification. These drivers remained the same in all regions, while idiosyncratic historical factors determined the timing and routes of dispersals.