Freshwater mussels (Bivalvia: Unionoida) are a species-rich group with biodiversity patterns strongly shaped by a life history strategy that includes an obligate parasitic larval stage. The subfamily Ambleminae represents the most diverse in Unionoida with over 340 species. Many amblemines have evolved specialized patterns of host use, which are associated with equally specialized host infection strategies. Using robust phylogenomic methods, we set out to reconstruct the evolution of life history traits in a clade of amblemines that have a suite of characters ostensibly adapted to infecting its molluscivorous host. Anchored hybrid enrichment and ancestral character reconstruction revealed a complex pattern of life history evolution with host switching and multiple instances of convergence, including reduction in size of larvae, increased fecundity, and growth during encapsulation. Our phylogenomic analyses also recovered non-monophyly of taxa exhibiting multiple traits used as the basis for previous taxonomic hypotheses. Taxa with axe-head shaped glochidia were resolved as paraphyletic, but our results strongly suggest the complex morphology is an adaptation to reduce larval size, with reduction in size further accentuated in taxa previously assigned to Leptodea. To more accurately reflect the evolutionary history of this group, we make multiple systematic changes, including the description of a new genus, Atlanticoncha gen. nov., and the synonymy of Leptodea under Potamilus. Our findings contribute to the growing body of literature showing that cladistic hypotheses based solely on morphological characters, including larval morphology, can be flawed in freshwater mussels.