Transient and low-affinity protein complexes pose a challenge to existing experimental methods and traditional computational techniques for structural determination. One example of such a disordered complex is that formed by trimers of influenza virus fusion peptide inserted into a host cell membrane. This fusion peptide is responsible for mediating viral infection, and spectroscopic data suggest that the peptide forms loose multimeric associations that are important for viral infectivity. We have developed an ensemble simulation technique that harnesses >1000 molecular dynamics trajectories to build a structural model for the arrangement of fusion peptide trimers. We predict a trimer structure in which the fusion peptides are packed into proximity while maintaining their monomeric structure. Our model helps to explain the effects of several mutations to the fusion peptide that destroy viral infectivity but do not measurably alter peptide monomer structure. This approach also serves as a general model for addressing the challenging problem of higher-order protein organization in cell membranes.