A molecular phylogeny of the family Paraonidae was reconstructed on the basis of 16S rDNA, COI and 18S rDNA sequences obtained from 66 individuals belonging to 38 nominal species and subspecies. In agreement with previous findings, Paraonidae represent a monophyletic group, closely related to Sternaspidae. The topology obtained by the Bayesian and Maximum Likelihood analyses on the combined dataset was not consistent with the traditional view on Paraonidae evolution, nor with a recent cladistic analysis. According to our results, Paraonidae are divided in five clades. The earliest branching clade (Clade I) included five species of the genera Cirrophorus and Paradoneis, whereas the remaining species of these genera were included in the Clade II. The genus Levinsenia is monophyletic and represents the sister group of a highly supported clade including some morphologically homogeneous species previously assigned to the genus Aricidea, which is here described as Blakeia n. gen. The remaining species of Aricidea clustered in a clade that included Paraonis as well. Paraonis can be interpreted as a pedomorphic form of Aricidea, accounting for the strong morphological divergence between the two genera. For priority rules, Aricidea should be considered a junior synonym of Paraonis. None of the subgenera traditionally recognised within Aricidea were monophyletic; in addition, the shallow molecular divergence identified among species, in particular for 18S rDNA sequences, suggests that the adaptive radiation of the genus Aricidea is relatively recent. Phylogenetic relationships suggested that the median antenna is an ancestral character, which has been independently lost several times, though a long, cirriform antenna only occurs in the genus Aricidea. The ancestral number of pre-branchial chaetigers is most likely three, even though arrangements with a higher number of chaetigers have been probably achieved at least twice independently. Notopodial modified chaetae appear to be a plesiomorphy of Paraonidae and they have been lost subsequently, whereas neuropodial modified chaetae have been acquired at least thrice independently through the evolutionary history of the family. Paraonidae show a strikingly high occurrence of cryptic and pseudocryptic species; results of the present work suggest that environmental features play a crucial role in the diversification of this family, whereas the influence of geographical distance appears less pronounced. Lastly, despite their importance in deep-water environments, Paraonidae probably are a primarily shallow-water family, that radiated in the deep sea secondarily.