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Abstract The recent advances in sequencing technologies, phylogenomics and divergence dating methods call for an integrative review of the current state of Hymenoptera systematics. We here explore the impact of these latest developments on the Hymenoptera phylogeny and our understanding of the timing of Hymenoptera evolution, while identifying the current methodological constraints and persistent knowledge gaps that warrant further investigation. Our review highlights the lack of consensus among the backbone phylogeny of Hymenoptera between key phylogenomic studies, as the higher level phylogeny remains unresolved in key nodes such as the relationships among Eusymphyta, the relationships within the Infraorder Proctotrupomorpha and the placements of the superfamilies Ichneumonoidea, Ceraphronoidea and Vespoidea. Furthermore, we underline the huge variation in divergence age estimates for Hymenoptera and detect several major gaps and/or disagreements between the fossil record and available age estimates, either due to the poorly studied fossil record or problematic age estimates, or both. To better understand the timing of Hymenoptera evolution and the role of key diversification factors, we will need continuous efforts to (i) reconcile conflicts among morphological and molecular phylogenies, by improving taxon sampling of underrepresented lineages, applying novel techniques to study morphology, making use of genome‐scale data and critically assessing incongruences in genetic markers; (ii) improve the Hymenoptera fossil record, by exercising integrative taxonomy and bringing together paleontologists and neontologists; and (iii) reconcile age estimates, by relying on tip dating approaches to bridge fossils, morphology and genomes across time.