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Abstract The Miltogramminae (Diptera: Sarcophagidae) includes ~600 species across >40 genera, which constitute ~20% of global Sarcophagidae. While molecular phylogenetic hypotheses have been produced for this group, critical problems persist, including the presence of paraphyletic genera, uncertain relationships between genera, a bias of sampling towards Palaearctic taxa, and low support for many branches. The present study remedies these issues through the application of Anchored Hybrid Enrichment (AHE) to a sample including ~60% of the currently recognised genera (16% of known species) representing all biogeographic regions except the Neotropical. An alignment of 1,281 concatenated loci was analysed with maximum likelihood (RAxML, IQ‐TREE), Bayesian inference (ExaBayes) and coalescent‐based approaches (ASTRAL, SVDquartets), which resulted in highly supported and concordant topologies, providing unprecedented insight into the relationships of this subfamily of flesh flies, allowing a major update to miltogrammine classification. The AHE phylogenetic hypothesis supports the monophyly of a large proportion of genera. The monophyly ofMetopiaMeigen is restored by synonymy withAenigmetopiaMalloch,syn.n.To achieve monophyly ofMiltogrammaMeigen, eight species are transferred fromPterellaRobineau‐Desvoidy. The genusPterellais shown to be paraphyletic in its current circumscription, and to restore generic monophylyPterellais restricted to contain onlyPt. grisea(Meigen).ErioproctaEnderlein,stat.rev., is resurrected. The genusSenotainiaMacquart is reconstructed as paraphyletic. The monotypic genusMetopodiaBrauer & Bergenstamm is synonymised withTaxigrammaMacquart,syn.n.In light of our phylogenetic hypotheses, a new Miltogramminae tribal classification is proposed, composed of six tribes.