Updated project metadata. Temperature passively affects many biological processes. It is therefore challenging to study dedicated temperature signalling pathways orchestrating plant thermomorphogenesis, a suite of elongation growth-based adaptations that enhance leaf cooling capacity. We screened a chemical library for compounds that restored abolished hypocotyl elongation in the pif4-2 deficient mutant background in the model plant Arabidopsis thaliana to identify novel regulators of thermomorphogenesis. The small aromatic compound ‘Heatin’, with 1-aminomethyl-2-naphthol as minimal active moiety, was isolated as potent enhancer of elongation growth. Following a chemical proteomics approach, the NITRILASE1-subfamily auxin biosynthesis enzymes were identified as molecular targets of Heatin. We show that Heatin inhibits NIT1-subfamily enzymatic activity and that accumulation of its substrate indole-3-acetonitrile (IAN) is sufficient for elongation growth in a NIT1-subfamily-dependent manner. Our work assigns a role for NITRILASE1-subfamily in mediating elongation growth. Moreover, Heatin and its functional analogues present novel chemical entities for understanding auxin biology.