Arabidopsis floral meristems terminate after the carpel primordia arise. This is achieved through the timed repression of WUSCHEL (WUS), which is essential for stem cell maintenance. At floral stage 6, WUS is repressed by KNUCKLES (KNU), a repressor directly activated by AGAMOUS (AG). KNU was suggested to repress WUS through histone deacetylation. However, how the changes in the chromatin state of WUS are initiated and maintained to terminate the floral meristem remains elusive. Here, we show that KNU integrates initial transcriptional repression with polycomb-mediated stable silencing of WUS. After KNU is induced, it binds to the WUS promoter and causes eviction of SPLAYED (SYD), which is a known activator of WUS and can act in opposition to polycomb repression. KNU also physically interacts with FERTILIZATION-INDEPENDENT ENDOSPERM (FIE), a key PRC2 component, and mediates the subsequent deposition of the repressive histone H3 lysine 27 tri-methylation (H3K27me3) for stable silencing of WUS. This multi-step silencing of WUS leads to the termination of floral stem cells, ensuring proper carpel development. Thus, our work describes a detailed mechanism for heritable floral stem cell termination in a precise spatiotemporal manner.