The evolutionary history of Ichneumoninae, the largest subfamily of ichneumonid wasps, is investigated using genomic ultraconserved elements (UCEs). The dataset includes 147 species in 130 genera of Ichneumoninae and 155 outgroup taxa from 19 subfamilies. Matrices with varying degrees of completeness were analysed with different partition schemes and the resulting topologies were found to be mostly congruent. All analyses recovered Ichneumoninae as a monophyletic group, sister to all other Ichneumoniformes except Agriotypinae. Almost no support was found for previous tribal classification schemes, except that the tribes Phaeogenini and Platylabini are largely monophyletic. A new tribal classification is proposed based on the relationships recovered, consisting of seven tribes: Alomyini Förster, Phaeogenini Förster, Notosemini Townes, Eurylabini Heinrich, Platylabini Berthoumieu, Ichneumonini Latreille and a new monogeneric tribe, Abzariini Santos & Wahl. As documented in other lineages of Ichneumonidae, pervasive morphological convergence poses a challenge to the establishment of higher-level groups that are both monophyletic and diagnosable. Extremely short branches at the base of the Ichneumoninae clade suggest that the group may have undergone a rapid radiation when it first diverged, potentially associated with its specialization on lepidopteran hosts. Multiple changes in the morphology of the female abdomen suggest that morphological convergence is associated with multiple transitions in the use of pupal versus larval hosts across the subfamily. The results demonstrate the power of phylogenomic approaches to resolve evolutionary relationships in hyper-diverse and poorly studied insect groups and to provide a framework for testing evolutionary hypotheses.