Maturation of omics and DNA barcode programs along with advances in sequence analysis tools and phyloinformatics protocols are enabling the realization of comprehensive and robust phylogenies of even the most diverse lineages. Several lineages in insects have undergone hyper‐radiations, and thus a unified picture of their evolution is ultimately required for understanding the process of diversification. In this study I further develop informatics protocols for de novo phylogenetic construction, and present the most species‐comprehensive insect phylogeny to date, constructed hierarchically using c. 440 transcriptomes, 1490 mitogenomes, DNA barcodes for 69 000 species, and several additional species‐rich markers. Even with this expanded transcriptome backbone, support is still insufficient for some historically problematic nodes, particularly in Polyneoptera and Paraneoptera. Low support (measured by internode certainty) was observed for the node separating Dictyoptera from its sister polyneopeterans; configuration of the Paraneoptera was not resolved; the recently proposed Hymenoptera grouping Eusymphyta received high support, while Parasitoida did not; and Orthorrhapha (Diptera) was not recovered. Sampling is uneven across the insects, and while highly sequenced lineages (e.g. Lepidoptera) boast greater information content, this accompanies computational burdens. The protocol and resulting tree represent an advance in the analytic and phylogenetic framework, for an objectively and consistently determined species‐comprehensive phylogeny.