The incorporation of synthetic polymers into biomolecular materials provides a powerful strategy to enhance their properties. We recently showed that the interstitial spaces of highly solvated mesoporous ferritin crystals could be infiltrated with acrylate (Ac) and acrylamide (Am) monomers, which are subsequently polymerized in crystallo to yield a new class of hybrid materials termed Polymer-Integrated Protein Crystals (PIX). Our earlier studies had shown that ferritin-PIX displayed remarkable properties such as reversible expansion and contraction without losing crystalline order, efficient self-healing, and the ability to encapsulate and release large biomolecular cargo. However, the structure of the polyacrylate-co-acrylamide (p(Ac-Am)) polymer matrix, its distribution within the protein lattice, and the molecular nature of the protein-polymer interactions that ultimately engender the emergent properties of ferritin-PIX have remained unknown. Here, we combine small-angle neutron and X-ray scattering and analytical measurements with extensive all-atom and coarse-grained molecular dynamics simulations to examine the structure and dynamics of the polymer network within the crystalline framework of ferritin-PIX. Our results reveal an extensive and multivariate set of noncovalent interactions between the ferritin surfaces and p(Ac-Am) chains that sustain the structural coherence of the crystalline lattice while accommodating large-scale motions. Guided by these insights, we have demonstrated that changes in the chemical compositions of ferritin and the polymer matrix can be used to predictably control the structural dynamics of ferritin-PIX. Our increased molecular-level understanding and engineering of the polymer-protein interface in ferritin-PIX provide an important step toward the generalization of the PIX concept to other protein crystals and polymer compositions.