Temperature is one of the most important perturbations for initiating the infectious phase of a virus as it is transmitted from a vector to host. Dengue serotype 2 shows a large expansion in viral capsid size at a temperature of 37 °C corresponding to the environment within the human host. Amide hydrogen/deuterium exchange mass spectrometry (HDXMS) is a powerful method to probe in parallel changes in dynamics across all constituent proteins in the viral capsid proteome at peptide resolution. Our results indicate that DENV2 viral particle shows high intrinsic and non-uniform dynamics across the C, E and M-proteins in the capsid and in alignment to the symmetry related contacts. These dynamic hotspots form the basis for where the largest changes are observed with temperature shift to 37 °C. These temperature-dependent changes in dynamics are largely irreversible and are specific to the viral particle. The breathing dynamics observed solely in whole viral assemblies highlight the importance of protein quaternary contacts, packing of lipid bilayer and RNA genome for the coordinated changes to temperature. The increased dynamics and temperature-dependent expansion measured by HDXMS expose hidden linear epitopes and modulate interactions with neutralizing antibodies. These results have enormous implications for targeted antibody discovery. HDXMS has also been applied to map antibody-whole viral complexes and allows a molecular understanding of antibody-dependent expansion.