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Abstract The genusLiriomyzaMik (Diptera: Agromyzidae) is a diverse and globally distributed group of acalyptrate flies. Phylogenetic relationships amongLiriomyzaspecies have remained incompletely investigated and have never been fully addressed using molecular data. Here, we reconstruct the phylogeny of the genusLiriomyzausing various phylogenetic methods (maximum likelihood, Bayesian inference, and gene tree coalescence) on target‐capture‐based phylogenomic datasets (nucleotides and amino acids) obtained from anchored hybrid enrichment (AHE). We have recovered tree topologies that are nearly congruent across all data types and methods, and individual clade support is strong across all phylogenetic analyses. Moreover, defined morphological species groups and clades are well‐supported in our best estimates of the molecular phylogeny.Liriomyza violivora(Spencer) is a sister group to all remaining sampledLiriomyzaspecies, and the well‐known polyphagous vegetable pests [L. huidobrensis(Blanchard),L. langeiFrick,L. bryoniae.(Kaltenbach),L. trifolii(Burgess),L. sativaeBlanchard, andL. brassicae(Riley)]. belong to multiple clades that are not particularly closely related on the trees. Often, closely relatedLiriomyzaspecies feed on distantly related host plants. We reject the hypothesis that cophylogenetic processes betweenLiriomyzaspecies and their host plants drive diversification in this genus. Instead,Liriomyzaexhibits a widespread pattern of major host shifts across plant taxa. Our new phylogenetic estimate forLiriomyzaspecies provides considerable new information on the evolution of host‐use patterns in this genus. In addition, it provides a framework for further study of the morphology, ecology, and diversification of these important flies.