Recent morphometric analysis revealed a juvenile (meraspid) axial growth gradient in the trunk of the ~429 Myr old trilobite Aulacopleura koninckii that resulted from growth control based on positional specification, as is common among extant organisms. Here we explore axial growth gradients in the more anterior body region, the cephalon, and in the cephalon and trunk during subsequent development in the holaspid period. We detected an axial growth gradient in the cephalon in the meraspid period, flatter and opposite in direction to that of the trunk, which also persisted during the holaspid period. We also found an holaspid trunk growth gradient, with a different distribution of growth rates among segments than that of the meraspid period. These newly observed growth gradients are compatible with the mechanism of growth control inferred for the meraspid trunk. Thus, the same kind of growth control may have operated in both body regions and during the whole ontogeny of A. koninckii. This study, along with others on the same species that preceded it, show that morphometric analysis of appropriate data sets can address questions of high interest for evolutionary developmental biology using data from fossils. By revealing developmental features at deep nodes of the phylogenetic tree, these studies will elucidate both how developmental processes evolved and how they themselves affected the evolution of organismal body patterning.