Conodonts constitute the earliest evidence of skeletal biomineralization in the vertebrate evolutionary lineage, manifest as a feeding apparatus of tooth-like elements comprised of enamel- and dentine-like tissues that evolved in parallel with these canonical tissues in other total-group gnathostomes. As such, this remarkable example of evolutionary parallelism affords a natural experiment in which to explore the constraints on vertebrate skeletal evolution. Using finite element analysis, informed by occlusal and microwear analyses, we tested the hypothesis that coincidence of complex dental function and microstructural differentiation in the enamel-like tissues of conodonts and other vertebrates is a consequence of functional adaptation. Our results show topological co-variation in the patterns of stress distribution and crystallite orientation. In regions of high stress, such as the apex of the basal cavity and inner parts of the platform, the crown tissue comprises interwoven prisms, discontinuities between which would have acted to decussate cracks, preventing propagation. These results inform a general occlusal model for platform conodont elements and demonstrate that the complex microstructure of conodont crown tissue is an adaptation to the dental functions that the elements performed.