G-quadruplexes (GQs) are guanine-rich, noncanonical nucleic acid structures that play fundamental roles in genomic stability and the regulation of gene expression. GQs are enriched in promoter sequences of growth regulatory genes and proto-oncogenes such as c-kit, which is linked to gastrointestinal stromal tumors, mast cell disease, and leukemia. While GQs have become a popular subject for experimental and computational research, the forces governing GQ dynamics are not fully understood. To gain insights into cation interactions and base-dipole moments of these highly ordered nucleic acid structures, we performed molecular dynamics simulations on the c-kit1 GQ using the CHARMM36 additive and Drude-2017 polarizable force fields. These simulations are the first of their kind to investigate the role of electronic polarization on interactions dictating GQ conformational sampling and cation interactions. Use of a polarizable model revealed differences in base dipole moments between GQs and B-form duplex DNA, force field-dependent ion binding pathways, and allowed for quantification of multibody contributions of water to ion-GQ interactions. These results emphasize the importance of electronic polarization as a contribution to the forces underlying nucleic acid dynamics.