Circadian rhythms are nearly ubiquitous throughout nature, suggesting they are critical for survival in diverse environments. Organisms inhabiting environments with arrhythmic days, such as caves, offer a unique opportunity to study the evolution of circadian rhythms in response to changing ecological pressures. Here we demonstrate that the cave environment has led to the repeated disruption of the biological clock across multiple populations of Mexican cavefish, with the circadian transcriptome showing widespread reductions in rhythmicity and changes to the timing of the activation/repression of genes in the core pacemaker. Then, we investigate the function of two genes with decreased rhythmic expression in cavefish. Mutants of these genes phenocopy reductions in sleep seen in multiple cave populations, suggesting a link between circadian dysregulation and sleep reduction. Altogether, our results reveal that evolution in an arrhythmic environment has resulted in dysregulation to the biological clock across multiple populations by diverse molecular mechanisms.