Peptides are commonly perceived as inapplicable components for construction of porous structures. Due to their flexibility the design is difficult and shape persistence of such putative structures is diminished. Notwithstanding these limitations, the advantages of peptides as building blocks are numerous: they are functional and functionalizable, widely available, diverse and biocompatible. We aimed at the construction of discrete porous structures that exploit the inherent functionality of peptides by an approach that is inspired by nature: structural pockets are defined by the backbones of peptides while functionality is introduced by their side chains. In this work peptide ribbons were preorganized on a macrocyclic scaffold using azapeptide-aldehyde reactions. The resulting cavitands with semicarbazone linkers arrange the peptide backbones at positions that are suitable for self-assembly of dimeric capsules by formation of binding motifs that resemble eight-stranded β-barrels. Self-assembly properties and inside/outside positions of the side chains depend crucially on the chirality of peptides. By rational optimization of successive generations of capsules we have found that azapeptides containing three amino acids in a (l, d, d) sequence give well-defined dimeric capsules with side chains inside their cavities. Taking advantage of the reversibility of the reaction of semicarbazone formation we have also employed the dynamic covalent chemistry (DCC) for a combinatorial discovery of capsules that could not be rationally designed. Indeed, the results show that stable capsules with side chains positioned internally can be obtained even for shorter sequences but only for combination peptides of (l, l) and (d, l) chirality. The hybrid (l, l)(d, l) capsule is amplified directly from a reaction mixture containing two different peptides. All capsules gain substantial ordering upon self-assembly, which is manifested by a two orders of magnitude increase of the intensity of CD spectra of capsules compared with non-assembled analogs. Temperature-dependent CD measurements indicate that the capsules remain stable over the entire temperature range tested (20-100 °C). Circular dichroism coupled with TD DFT calculations, DOSY measurements and X-ray crystallography allow for elucidation of the structures in the solid state and in solution and guide their iterative evolution for the current goals.