Recent molecular phylogenetic investigations strongly supported placement of the shell-less, worm-shaped aplacophoran molluscs (Solenogastres and Caudofoveata) and chitons (Polyplacophora) in a clade called Aculifera, which comprises the sister taxon of all other molluscs. Thus, understanding the evolutionary history of aculiferan molluscs is important for understanding early molluscan evolution. In particular, many basic questions about the systematics of Aplacophora have long been unanswered. Here, we supplemented the paucity of available data with transcriptomes from 25 aculiferans and conducted phylogenomic analyses on datasets with up to 525 genes. Our results indicate that aplacophoran taxonomy is in need of revision as several traditionally recognized groups are non-monophyletic. Most notably, Cavibelonia, the solenogaster taxon defined by hollow sclerites, is polyphyletic, suggesting loss of hollow sclerites in multiple taxa. Moreover, we describe Apodomenia enigmatica, a bizarre new species that appears to be a morphological intermediate between Solenogastres and Caudofoveata. However this animal is not a missing link molecular and morphological studies show that it is a remarkable, derived solenogaster that lacks a foot, mantle cavity, and radula. Taken together, these results shed light on the evolutionary history of Aplacophora and reveal a surprising degree of morphological plasticity within the group. Additional details on specimen collection localities are available in the publication or from Kevin Kocot.