The nucleosome core particle (NCP) is the basic packaging unit of DNA. Recently reported structures of the NCP suggest that the histone octamer undergoes conformational changes during the process of DNA translocation around the histone octamer. Herein, we demonstrate with long-time all-atomistic molecular dynamics simulations that the histone tails play a critical role in this nucleosome repositioning. We simulate the NCP at high salt concentrations, an order of magnitude higher than physiological conditions, to screen the electrostatic interactions. We find that the positively charged H2B tail collapses and complexes with the minor groove of nucleosomal DNA. Upon collapse of the tail, counterions are released. This promotes the formation of a ∼10 bp loop of nucleosomal DNA. The complexation of the tail increases the local flexibility of the DNA, as characterized by local force constants. Using normal mode analysis, we identify a "wave-like motion" of nucleosomal DNA. We perform umbrella sampling to characterize two possible pathways of the initial stages of unwrapping, symmetric and asymmetric. These results suggest that regulation of the histone tail interactions with nucleosomal DNA may play a critical role in nucleosomal dynamics by acting as a switch to determine the initial pathway of unwrapping.