Comprising over half of all described species, the hexapods are central to understanding the evolution of global biodiversity. Direct fossil evidence suggests that new hexapod orders continued to originate from the Jurassic onwards, and diversity is presently higher than ever. Previous studies also suggest that several shifts in net diversification rate have occurred at higher taxonomic levels. However, their inferred timing is phylogeny dependent. We re-examine these issues using the supertree approach to provide, to our knowledge, the first composite estimates of hexapod order-level phylogeny. The Purvis matrix representation with parsimony method provides the most optimal supertree, but alternative methods are considered. Inferring ghost ranges shows richness of terminal lineages in the order-level phylogeny to peak just before the end-Permian extinction, rather than the present day, indicating that at least 11 more lineages survived this extinction than implied by fossils alone. The major upshift in diversification is associated with the origin of wings/wing folding and for the first time, to our knowledge, significant downshifts are shown associated with the origin of species-poor taxa (e.g. Neuropterida, Zoraptera). Polyneopteran phylogeny, especially the position of Zoraptera, remains important resolve because this influences findings regarding shifts in diversification. Our study shows how combining fossil with phylogenetic information can improve macroevolutionary inferences.