<p>Apicomplexans are a diverse phylum of single-celled protists that are all obligate animal symbionts. The most well-studied members are severe pathogens of humans and livestock, such as the causative agents of malaria, cryptosporidiosis, toxoplasmosis, and coccidiosis, but comparatively little is known about their invertebrate-infecting counterparts, which are evolutionarily and ecologically important, but often overlooked. One of these groups is the Cephaloidophoroidea gregarine superfamily which is one of the most often-detected apicomplexan groups in molecular surveys of marine environments. The few members that have been isolated and molecularly characterized primarily infect crustaceans, and indeed all known crustacean-infecting gregarines phylogenetically branch within the Cephaloidophoroidea. Here we expand the phylogenomic data for gregarines from crustacean hosts, report 11 new species of crustacean-infecting gregarines, and perform phylogenomic analyses using transcriptome data to determine their position on the tree of Apicomplexa. The crustacean-infecting gregarines primarily do branch with the Cephaloidophoroidea, but not exclusively. <i>Lentusidium euphilomedae</i> n. gen. et sp., found in the seed shrimp <i>Euphilomedes</i> sp., branches very distantly to the Cephaloidophoroidea forming a strongly supported sister to Lecudinoidea. We show that crustacean-infecting gregarines comprise multiple evolutionary lineages providing important context for future interpretations of marine environmental surveys.</p>