This study explores the dynamic and hierarchical structural organization of peptide coacervate microdroplets at the meso- to atomic-scale resolution using a combination of Transferred Nuclear Overhauser Effect Spectroscopy (TrNOESY), small-angle neutron scattering (SANS) with selective deuteration, and confocal microscopy. It presents the application of the established TrNOESY technique to the study of peptide-based coacervates, a previously unexplored context. This approach enables direct, high-resolution detection of residue-level interactions within the intact droplets. Dynamic interactions driving the self-association of peptide clusters are revealed, highlighting the critical roles of interacting residues. These phase-separating model peptides form small oligomers at low pH, which self-associate into peptide clusters at neutral pH and organize into a porous network within the droplets, facilitating size-selective cargo sequestration. The findings underscore the significance of the dynamic spatiotemporal properties of peptide-based coacervates, contributing to our understanding of phase separation at the atomic and molecular levels. Critically, this approach enables the investigation of coacervate structures in their native state, offering insights into the physical and dynamic interactions governing droplet formation and cargo encapsulation.