Biomineralization in vertebrates is a ubiquitous and tightly regulated process which creates hierarchical structures for the skeleton. Because of the lack of understanding and applicability of cell-based or biological systems to achieve intrafibrillar mineralization, scientists adopted various in vitro methods to elucidate the mechanism of intrafibrillar mineralization. In this article, biomimetic intrafibrillar mineralization of collagen in its wide ramifications is reviewed. It is intriguing how prevailing intrafibrillar mineralization mechanisms derived from two potentially discordant crystallization philosophies were equally adept, depending on the experimental context, at theorizing the formation of calcium phosphate within a fibrillar template. This complementarity is not unique to biomineralization and has precedence in other fundamental physical interpretations. A new intrafibrillar mineralization process based on the use of polycationic process-directing agent added uncertainty to the use of existing mechanisms in accounting for the observations.