Self-assembling peptides have been previously designed that assemble into macroscopic membranes, nanotapes, and filaments through electrostatic interactions. However, the formation of highly ordered collagen-like fibrils, which display D-periodic features, has yet to be achieved. In this report, we describe for the first time a synthetic peptide system that self-assembles into a fibrous structure with well-defined periodicity that can be visualized by transmission electron microscopy (TEM). Specifically, we designed and synthesized a peptide that utilizes charged amino acids within the ubiquitous Xaa-Yaa-Gly triad sequence to bias the self-assembly into collagen-like homotrimeric helices that are capable of fibrillogenesis with the production of D-periodic microfibers. Potential molecular mechanisms for peptide assembly into triple-helical protomers and their subsequent organization into structurally defined, linear assemblies were explored through molecular dynamics (MD) simulations. The formation of thermodynamically stable complexes was attributed to the presence of strong electrostatic and hydrogen bond interactions at staggered positions along the linear assembly. This unexpected mimicry of native collagen structure using a relatively simple oligopeptide sequence establishes new opportunities for engineering linear assemblies with highly ordered nano- and microscale periodic features. In turn, the capacity to precisely design periodic elements into an assembly that faithfully reproduces these features over large length scales may facilitate the fabrication of ordered two- and three-dimensional fiber networks containing oriented biologically, chemically, or optically active elements.