Emulating the multiple facets of metalloprotein coordination into a model system has been a long-standing goal. One strategy has been to increase the size and complexity of small molecule ligands, but this generally requires time-intensive and laborious organic syntheses. Alternatively, by leveraging self-assembly, metal-organic frameworks (MOFs) have emerged as a promising strategy for metalloprotein mimicry. In MOFs, metal ions are assembled with ligands to generate a lattice containing substrate-accessible pores. Because the metal sites are immobilized in MOFs, they are protected from intermolecular deactivation pathways. Furthermore, MOFs tend to utilize ligands bearing carboxylate and N-heterocyclic donors that resemble weak-field protein-based donors. Indeed, MOFs have enabled unique metal-based reactivity that is rarely achieved by homogeneous complexes, such as stabilization of coordinatively unsaturated metal sites and terminal oxo ligands. By exploiting the same amino acid building blocks as proteins, metal-peptide frameworks (MPFs) could significantly increase the biological similarity of porous framework model systems. However promising, the rational design of MPFs is underdeveloped, and there remains a large gap in the application of peptides in forming porous materials. Di-and tripeptides are most commonly used to synthesize MPFs, since their short chain lengths have fewer rotational degrees of freedom, making them conducive to consistent framework formation. Frameworks built from longer peptide sequences are very scarce as they require careful designs to control the peptide secondary structure, and the known examples employ unnatural metal-binding motifs. But MPFs in contrast, form with secondary structure and can bind to metals solely via canonical amino acid sidechains, as would be desired for accurate biomimicry, which has only just been reported by Lee and co-workers in 2023. There, they showed that short foldamer-based helixes incorporating two methionine residues can generate porous frameworks with copper(I) iodide clusters. However, MPFs made from peptide linkers with secondary structure that chelate metal sites with the more ubiquitous aspartate, glutamate, and histidine sidechains are needed. Here, we report a highly general strategy using small α-helical peptides that generates a range of site-isolated biomimetic metal sites coordinated to canonical metal-binding amino acid residues. We develop a point mutation strategy that can produce a variety of metal coordination spheres and dynamics, demonstrating the high level of tunability of these metal-α-helix peptide frameworks.