Many bacteria, including the model bacterium Escherichia coli can survive for years within spent media, following resource exhaustion. We carried out evolutionary experiments, followed by full genome sequencing of hundreds of evolved clones to study the dynamics by which E. coli adapts during the first four months of survival under resource exhaustion. Our results reveal that bacteria evolving under resource exhaustion are subject to intense selection, manifesting in rapid mutation accumulation, enrichment in functional mutation categories and extremely convergent adaptation. Our results further demonstrate that such adaptation is not limited by mutational input. Indeed, adaptation under conditions of resource exhaustion is rapid enough to enable bacteria to temporally regulate their gene expression and metabolism, at the population level, via genetic modifications. Finally, we demonstrate that due to antagonistic pleiotropy and mutation accumulation, survival under resource exhaustion can severely reduce a bacterium’s ability to grow exponentially, once resources are again available.