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Endocytosis regulates the turnover of cell surface localized receptors, which are crucial for plants to rapidly respond to stimuli. The evolutionary ancient TPLATE complex (TPC) plays an essential role in endocytosis in Arabidopsis plants. Knockout or knockdown of single TPC subunits causes male sterility and seedling lethality phenotypes, complicating analysis of the roles of TPC during plant development. Partially functional alleles of TPC subunits however only cause mild developmental deviations. Here, we took advantage of the partially functional TPLATE allele, WDXM2, to investigate a role for TPC‐dependent endocytosis in receptor‐mediated signaling. We discovered that reduced TPC‐dependent endocytosis confers a hypersensitivity to very low doses of CLAVATA3 peptide signaling. This hypersensitivity correlated with the abundance of the CLAVATA3 receptor protein kinase CLAVATA1 at the plasma membrane. Genetic and biochemical analysis as well as live‐cell imaging revealed that TPC‐dependent regulation of CLAVATA3‐dependent internalization of CLAVATA1 from the plasma membrane is required for shoot stem cell homeostasis. Our findings provide evidence that TPC‐mediated endocytosis and degradation of CLAVATA1 is a mechanism to dampen CLAVATA3‐mediated signaling during plant development. Synopsis: A slight reduction in endocytic capacity, caused by a partially functional TPLATE complex, confers a hypersensitivity to very low doses of CLAVATA3‐type peptide signaling correlating with the abundance of the receptor protein kinase CLAVATA1 at the plasma membrane. Genetic, biochemical, and live‐cell imaging analysis reveals that TPLATE complex‐dependent internalization of CLAVATA1 from the plasma membrane is required for shoot stem cell homeostasis. Plants expressing a partially functional TPLATE complex are hypersensitive to exogenous CLAVATA3‐type peptides.The hypersensitivity to CLAVATA3‐type peptide signaling correlates with an increased abundance of the CLAVATA1 receptor at the plasma membrane.TPLATE complex‐dependent regulation of CLAVATA1 internalization is required to dampen CLAVATA3‐mediated signaling during plant development.The AtEH1/Pan1 subunit of the TPLATE complex interacts with the cytoplasmic tail of the CLAVATA1 receptor. [ABSTRACT FROM AUTHOR]