<jats:title>Summary</jats:title><jats:p>Sedentary plant‐parasitic cyst nematodes are obligate biotrophs that infect the roots of their host plant. Their parasitism is based on the modification of root cells to form a hypermetabolic syncytium from which the nematodes draw their nutrients. The aim of this study was to identify nematode susceptibility genes in <jats:italic>Arabidopsis thaliana</jats:italic> and to characterize their roles in supporting the parasitism of <jats:italic>Heterodera schachtii</jats:italic>. By selecting genes that were most strongly upregulated in response to cyst nematode infection, we identified HIPP27 (<jats:italic>H</jats:italic>EAVY METAL‐ASSOCIATED <jats:italic>I</jats:italic>SOPRENYLATED <jats:italic>P</jats:italic>LANT <jats:italic>P</jats:italic>ROTEIN <jats:italic>27</jats:italic>) as a host susceptibility factor required for beet cyst nematode infection and development. Detailed expression analysis revealed that HIPP27 is a cytoplasmic protein and that <jats:italic>HIPP27</jats:italic> is strongly expressed in leaves, young roots and nematode‐induced syncytia. Loss‐of‐function Arabidopsis <jats:italic>hipp27</jats:italic> mutants exhibited severely reduced susceptibility to <jats:italic>H. schachtii</jats:italic> and abnormal starch accumulation in syncytial and peridermal plastids. Our results suggest that <jats:italic>HIPP27</jats:italic> is a susceptibility gene in Arabidopsis whose loss of function reduces plant susceptibility to cyst nematode infection without increasing the susceptibility to other pathogens or negatively affecting the plant phenotype.</jats:p>