G-quadruplexes (GQs) are highly stable noncanonical forms of nucleic acids that are present in important genomic regions. The central core of the GQ is lined up by four closely spaced carbonyl groups from the G-quartets, and the resulting electrostatic repulsion is neutralized by the coordinating cations. In spite of several reports on GQ structure and cation-GQ interactions, the atomic- to molecular-level understanding of the ion dynamics and ion exchange in the GQ core is quite poor. Here, we attempt to elucidate the mechanism of Na+ and K+ binding to the GQ core and trace the exchange of these ions with the ions in bulk by means of all-atomic molecular dynamics (MD) simulations. One of the most studied GQs, Oxytricha nova telomeric G-quadruplex (OxyGQ), is taken as the representative GQ Subsequently, umbrella sampling MD simulations were performed to elucidate the energetics of ion translocation from one end to the other end of the GQ central core. Our study highlights the importance of ion hydration for the uptake and correct positioning of the cations in the core. The free-energy landscape of ion transport has shown favorable in-plane binding of Na+ ions with GQ quartets, which matches very well with the crystal structure. The binding of K+ ions, on the other hand, was out-of-plane and its translocation required a larger barrier to cross.