How eukaryotic cells assess and maintain sizes specific for their species and cell type remains unclear. We show that in the Arabidopsis shoot stem cell niche, cell size variability due to asymmetric divisions is corrected by adjusting the growth period before DNA synthesis. KIP-related protein 4 (KRP4) inhibits progression to DNA synthesis and associates with mitotic chromosomes. The F BOX-LIKE 17 (FBL17) protein removes excess KRP4. Consequently, daughter cells are born with comparable amounts of KRP4. Inhibitor dilution models predicted that KRP4 inherited via chromatin would robustly regulate size, whilst inheritance of excess free KRP4 would disrupt size homeostasis, as confirmed by mutant analyses. We propose that a cell cycle regulator, stabilized by association with mitotic chromosomes, reads DNA content as a cell size-independent scale.