In flowering plants, the switch from floral stem cell maintenance to gynoecium (female structure) formation is a critical developmental transition for reproductive success. In Arabidopsis thaliana, AGAMOUS (AG) terminates floral stem cell activities to trigger this transition. Although CRABS CLAW (CRC) is a direct target of AG, previous research has not identified any common targets. Here, we identify an auxin synthesis gene, YUCCA4 (YUC4) as a common direct target. Ectopic YUC4 expression partially rescues the indeterminate phenotype and cell wall defects that are caused by the crc mutation. The feed-forward YUC4 activation by AG and CRC directs a precise change in chromatin state for the shift from floral stem cell maintenance to gynoecium formation. We also showed that two auxin-related direct CRC targets, YUC4 and TORNADO2, cooperatively contribute to the termination of floral stem cell maintenance. This finding provides new insight into the CRC-mediated auxin homeostasis regulation for proper gynoecium formation.