For more than a century, the origin and evolution of the arthropod head and brain have eluded a unifying rationale reconciling divergent morphologies and phylogenetic relationships. Here, clarification is provided by the fossilized nervous system of the lower Cambrian lobopodian Cardiodictyon catenulum, which reveals an unsegmented head and brain comprising three cephalic domains, distinct from the metameric ventral nervous system serving its appendicular trunk. Each domain aligns with one of three components of the foregut and with a pair of head appendages. Morphological correspondences with stem group arthropods and alignments of homologous gene expression patterns with those of extant panarthropods demonstrate that cephalic domains of C. catenulum predate the evolution of the euarthropod head yet correspond to neuromeres defining brains of living chelicerates and mandibulates.