The nucleolus is a phase separated compartment formed from proteins and RNA during interphase in eukaryotes as the site of ribosome biogenesis. Nucleoli have slow viscoelastic condensate dynamics that are currently not well captured by in vitro models. We show that an interplay between magnesium ions (Mg2+) and ATP ultimately shapes both the dynamics and the physical state of an in vitro nucleolus model of nucleophosmin 1 (NPM1) protein and ribosomal RNA (rRNA), as well as ribosomes themselves. NPM1 is essential for the nucleation of NPM1-rRNA condensates. At high free Mg2+ concentrations, rRNA is fully arrested and the condensates are gels, whereas NPM1 remains mobile. Using quantitative fluorescence microscopy, we show that the NPM1-rRNA droplets can ‘age’ and that RNA compaction is temperature-reversible, indicating that RNA-RNA interactions contributes to the slowed dynamics. The dynamic arrest of RNA can be reversed by ATP, resulting in complete liquefaction of previous gel-like structures and differences in partitioning of client proteins and RNAs. In fact, we show that an intriguing ribosome halo appears around the NPM1-rRNA condensates when Mg2+ concentrations exceed ATP concentrations, reminiscent of nucleoli function. Within cells, ATP levels are controlled by biomolecular reactions, and we demonstrate that dissipative enzymatic networks can similarly control the biophysical properties of in vitro condensates through depletion of ATP using apyrase. Our results illustrate how cells could regulate the dynamics of RNA-based condensates, such as the nucleolus.