Bone is a natural biocomposite with an intricate, hierarchical organization that results in structural properties ideal for protecting and supporting the body’s soft tissues. For more effective treatment of severe bone injuries, which affect millions of people worldwide, we need implantable scaffolds that can replace bone’s supportive function while facilitating regeneration of new bone at the implant site. Synthetic fibers that can mimic the nanostructure of natural bone show promise to replicate bone’s structural and biological function, yet few materials have been able to recreate the precise mineral organization of bone. In particular, control over the spatial distribution and orientation of mineral crystals in fibers remains a challenge for biomimicry. In order to achieve this, a method is needed to guide mineralization to occur with periodic distribution and alignment within a polymeric matrix. The objective of this work is to direct the biomineralization of a nanofibrous scaffold using hierarchically nanostructured polymers. We achieve this by using poly(acrylic acid) (PAA) as a recruiter of calcium ions to initiate the nucleation and growth of hydroxyapatite within a poly(caprolactone) (PCL) scaffold. To create the hierarchical composite, we crystallize a block copolymer of PCL-b-PAA onto the surface of electrospun PCL nanofibers. This creates a nanofiber shish-kebab morphology that nucleates hydroxyapatite into periodic PAA domains for a repeating mineral structure with orientation induced by nanoscale confinement. We have shown that calcium phosphate will form within nanoscale PAA domains first as an amorphous calcium phosphate phase before crystallizing into hydroxyapatite. Wide-angle X-ray diffraction and transmission electron microscopy have been used to confirm that the mineral crystals form in repeating lamellae oriented perpendicular to the fiber backbone. By altering the copolymer domain location and size, we direct the formation kinetics, orientation, and amount of minerals in the composite. PAA can additionally be incorporated into the nanofiber backbones for further possible mineral content and structure. Compared to other mineralization-directing techniques such as surface modification and polymer-induced liquid precursors, our block copolymer-directed mineralization gives us greater control over the possible composite morphologies that can be achieved. Through this system, we more closely mimic the nanoscale bone structure to achieve better mechanical performance.