Scarce and controversial information on visual organs and their innervation in Onychophora currently do not allow a thorough comparison with Euarthropoda. Therefore, this study sets out to provide additional data on the architecture and morphogenesis of the onychophoran visual system and to explore similarities and differences between the visual organs of onychophorans and other arthropods. Based on the new data for Epiperipatus biolleyi (Peripatidae) and Metaperipatus blainvillei (Peripatopsidae), it is suggested that the compound eyes represent an autapomorphy of Euarthropoda since similarities with the onychophoran eyes are weak or absent. Instead, the innervation from a central rather than lateral part of the brain, the presence of only one (paired or unpaired) visual center, and a similar ontogenetic origin from an ectodermal groove rather than a proliferation zone suggest homology between the onychophoran eyes and the median ocelli of euarthropods. In conclusion, I suggest that the last common ancestor of arthropods bore only one pair of ocellus-like visual organs that were modified in several arthropod lineages. This hypothesis is supported by recent paleontological data.