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, mutational input appears to be high enough to enable bacteria to rapidly adapt, in a highly convergent manner and with great temporal precision through fluctuations in allele frequencies. 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. We study how this affects the ability of bacterial populations to re-adapt to growth once resources again become available. Combined, our results shed light on bacterial adaptation to long-periods of resource exhaustion and on the consequences such adaptation has on the genetic makeup of individual bacteria and on patterns of genetic variation within bacterial populations.