Muller's ratchet refers to the irreversible accumulation of deleterious mutations in small populations, resulting in a decline in overall fitness. This phenomenon has been extensively observed in experiments involving microorganisms, including bacteriophages and yeast. While the impact of Muller’s ratchet on viruses has been largely studied in bacteriophages and animal RNA viruses, its effects on plant RNA viruses remain poorly documented. Plant RNA viruses give rise to large and diverse populations that undergo significant bottlenecks during the colonization of distant tissues or through vector-mediated horizontal transmission. In this study, we aim to investigate the role of bottleneck size, the maximum population size between consecutive bottlenecks, and the generation of genetic diversity in countering the effects of Muller’s ratchet. We observed three distinct evolutionary outcomes for tobacco etch virus under three different demographic conditions: ( i ) a decline in fitness following periodic severe bottlenecks in Chenopodium quinoa , ( ii ) a consistent fitness level with moderate bottlenecks in C. quinoa , and ( iii ) a net increase in fitness when severe bottlenecks in C. quinoa were alternated with large population expansions in Nicotiana tabacum . By fitting empirical data to an in silico simulation model, we found that initiating a lesion in C. quinoa required only 1-5 virions, and approximately 40 new virions were produced per lesion. These findings demonstrate that Muller's ratchet can be halted not only by increasing the number of founder viruses but also by incorporating phases of exponential growth to large populations between bottlenecks. Such population expansions generate genetic diversity, serving as a buffer against, and potentially even leveraging, the effects of genetic drift.