Self-assembled aggregates of peptides containing aromatic groups possess optoelectronic properties that make them attractive targets for the fabrication of biocompatible electronics. Molecular-level understanding of the influence of microscopic peptide chemistry on the properties of the aggregates is vital for rational peptide design. In this study, we construct a coarse-grained model of Asp-Phe-Ala-Gly-OPV3-Gly-Ala-Phe-Asp (DFAG-OPV3-GAFD) peptides containing OPV3 (distyrylbenzene) pi-conjugated cores explicitly parameterized against all-atom calculations and perform molecular dynamics simulations of the self-assembly of hundreds of molecules over hundreds of nanoseconds. We observe a hierarchical assembly mechanism, wherein approximately two to eight peptides assemble into stacks with aligned aromatic cores that subsequently form elliptical aggregates and ultimately a branched network with a fractal dimensionality of similar to 1.5. The assembly dynamics are well described by a Smoluchowski coagulation process, for which we extract rate constants from the molecular simulations to both furnish insight into the microscopic assembly kinetics and extrapolate our aggregation predictions to time and length scales beyond the reach of molecular simulation. This study presents new molecular-level understanding of the morphology and dynamics of the spontaneous self-assembly of DFAG-OPV3-GAFD peptides and establishes a systematic protocol to develop coarse-grained models of optoelectronic peptides for the exploration and design of pi-conjugated peptides with tunable optoelectronic properties.