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ABSTRACT While many plant lineages display remarkable diversity in morphological form, our understanding of how phenotypic diversity, or disparity, arises in relation to genomic evolution over geologic scales remains poorly understood. Here, we investigated the relationship between phenotypic and genomic evolution in the Fagales, a lineage of woody plants that has been a dominant component of temperate and subtropical forests since the Late Cretaceous. We examine newly generated transcriptomic and trait datasets representing most extant genera and a rich diversity of Cretaceous fossil representatives. Our phylogenomic analyses identify recurrent hotspots of gene duplication and genomic conflict across the order. Our phenotypic analyses showed that the morphospace occupied by Fagales was largely filled by the early Cenozoic, and rates of evolution were highest during the early radiation of the Fagales crown and its major families. These results suggest that Fagales conforms to an “early‐burst” model of disparification, with morphospace being filled early in the order's diversification history, and that elevated levels of phenotypic evolution also often correspond to hotspots of gene duplication. Species diversification appears decoupled from patterns of both phenotypic and genomic evolution, highlighting the multidimensional nature of the evolution of plant diversity across geological timescales.