Adaptations to high latitude photoperiods have been under positive selection during the domestication of many short-day (SD) flowering crops. Photoperiod insensitivity (auto-flowering) in drug-type Cannabis sativa circumvents the need for SD flowering requirements making outdoor cultivation in high latitudes possible. However, the benefits of photoperiod insensitivity are counterbalanced by low cannabinoid contents and poor flower quality in auto-flowering genotypes. Despite recent legalization in some countries, a mechanistic understanding of photoperiod insensitivity in cannabis is still lacking. Herein, we identify a splice site mutation within PSEUDO-RESPONSE REGULATOR 37 (CsPRR37) in auto-flowering cannabis that causes photoperiod insensitivity. Using a combination of GWAS, fine mapping, and gene expression analyses, our results strongly indicate CsPRR37 as the most likely candidate for causing photoperiod insensitivity. Research into the pervasiveness of this mutation and others effecting flowering time will help elucidate its domestication history and advance cannabis breeding towards a more sustainable outdoor cultivation system.