Ctenostome bryozoans pose ongoing challenges for taxonomists and systematists, owing to their lack of character-rich mineralized skeletons. We present the largest (super)family-level phylogeny of Ctenostomatida to date. We resolved the three major clades (A–C) that were recognized previously. Clade A included endolithic taxa Penetrantiidae, Immergentiidae, and Terebripora ramosa, the latter two being sister taxa. Other taxa in this clade were Nolella, Arachnidium, Pottsiella, and Paludicella. Clade B was composed of Alcyonidioidea and Multiporata. The genus
Alcyonidium was revealed as non-monophyletic, with the two recovered clades likely to be characterized by contrasting reproductive modes (brooding and zygote spawning). Members of the presumptive brooding clade had insertions of possible exogenous origin in their 18S and 28S ribosomal RNA genes, which might be the result of horizontal gene transfer. Clade C was sister to the Cheilostomatida and was composed of Vesicularioidea, Hislopioidea, Walkerioidea, and three clades of Victorellidae. Anguinella and Hypophorella were consistently sister taxa, but their
position was unstable. Results are discussed in light of morphology, reproduction, and previous phylogenetic hypotheses. A revised classification is proposed. Timwoodiellina natans is transferred to Hislopia, Vesicularia spinosa to Amathia, and Monobryozoon ambulans to Alcyonidium. Members of the putative zygote-spawning Alcyonidium clade are transferred to Alcyonidioides in the family Alcyonidioididae.