Petal senescence refers to the progressive loss of intracellular structures and functions within plant decorative organs, ultimately leading to cell death. Autophagy involves the degradation of damaged cellular components and nutrient recycling. Plant organ senescence and autophagy are highly coordinated; however, the mechanisms by which autophagy regulates petal senescence remain largely unknown. In this study, by using transmission electron microscopy, we observed that autophagic activity peaked early, at flower opening, without any senescence and other morphological symptoms in petals. We found that darkness positively regulated petal senescence and upregulated autophagy-related genes (ATGs). Dark treatment promoted the accumulation of Rosa hybrida phytochrome-interacting factor 4 ( RhPIF4) in petals. RhPIF4 silencing delayed petal senescence and repressed the expression of ATGs. In contrast, silencing of the light-responsive gene Rosa hybrida elongated hypoctyl 5 ( RhHY5) promoted petal senescence and ATG gene expression. RhPIF4/8 and RhHY5 could directly interact with RhWRKY40, and RhWRKY40 is directly bound to the promoters of RhATG7 and RhATG11. Silencing RhWRKY40 delayed petal senescence and suppressed RhATG7 and RhATG11 expression. Based on these results, we propose that RhPIF4/8 and RhHY5 transcription factors are involved in regulating petal senescence in response to dark or light conditions by modulating autophagic activity.