Sea scorpions (Eurypterida, Chelicerata) of the Lower Devonian (~400 Mya) lived as large, aquatic predators. The structure of modern chelicerate eyes is very different from that of mandibulate compound eyes [Mandibulata: Crustacea and Tracheata (Hexapoda, such as insects, and Myriapoda)]. Here we show that the visual system of Lower Devonian (~400 Mya) eurypterids closely matches that of xiphosurans (Xiphosura, Chelicerata). Modern representatives of this group, the horseshoe crabs (Limulidae), have cuticular lens cylinders and usually also an eccentric cell in their sensory apparatus. This strongly suggests that the xiphosuran/eurypterid compound eye is a plesiomorphic structure with respect to the Chelicerata, and probably ancestral to that of Euchelicerata, including Eurypterida, Arachnida and Xiphosura. This is supported by the fact that some Palaeozoic scorpions also possessed compound eyes similar to those of eurypterids. Accordingly, edge enhancement (lateral inhibition), organised by the eccentric cell, most useful in scattered light-conditions, may be a very old mechanism, while the single-lens system of arachnids is possibly an adaptation to a terrestrial life-style.