The capsid of cowpea chlorotic mottle virus (CCMV) can reversibly switch between two forms that are contingent on the charge of acidic residues that are clustered at the quasi-threefold axes of the T=3 icosahedral particle. The quaternary structure conformations are dependent on divalent metal ions and pH and were previously analyzed by crystallography in the native, compact form, and by cryo-electron microscopy in the compact and swollen forms (Speir et al., 1995). In this report we use the atomic models of the three structurally unique viral subunits determined by crystallography for a detailed interpretation of the 28-A-resolution electron density of the swollen form and the production of a pseudo-atomic model of this particle. The model of the quaternary structure conforms with high fidelity to conventional geometric constraints, quasi-equivalence, intersubunit association energies, and the electron density. It was derived by conserving the pentamers and hexamers of subunits whose associated electron densities are strikingly similar in the two forms of the particles. Treating these as rigid units in the modeling implies that the particle flexibility is accommodated primarily by changes in dimer interactions, an observation that is consistent with the flexible C-terminal polypeptide extensions that stabilize this contact in the crystal structure. Because the hexamers and pentamers were incrementally translated and rotated in a screw motion, with energy minimization at each of 28 steps, a path for the expansion is also implied.