The termination of floral meristems is regulated by the MADS domain transcription factor AGAMOUS (AG) by passively diluting the H3K27me3 mark along the KNUCKLES (KNU) coding sequence. How many other downstream genes are similarly regulated by this intrinsic epigenetic timer and whether it can be harnessed for engineering synthetic circuits are unknown. Here, we describe a biotimer gene regulatory network downstream of AG and manipulate the timing of KNU expression through a synthetic system. We manipulated temporal gene expression using the del region from the KNU coding sequence, which is decorated by H3K27me3-marked nucleosomes. Increasing the number of del copies delayed and reduced KNU expression in a PRC2- and cell cycle-dependent manner. We propose that PRC2 deposits H3K27me3, while cell divisions dilute H3K27me3 accumulation on the extended KNU coding sequence. Our results shed light on temporal transitions governing flower development and provide a novel tool for tunable gene expression.