Corky root rot is a ubiquitous soil-borne disease of tomato caused by the pathogen Pyrenochaeta lycopersici. This filamentous fungus is found on the roots of many crops and can persist in the soil up to 15 years as microsclerotia. High prevalence of corky root rot can be partly explained by the endurance and the broad host range of P. lycopersici, but how this fungus can gain access to host roots is still poorly understood, as its competitive saprophytic ability is very low. We have combined microscopy and reporter gene techniques to investigate the tomato-P. lycopersici interaction in vitro, and discovered the pathogen secretes molecules that change the direction of root growth and induce cell necrosis specifically in the apical part of the root of tomato ( apex, elongation zone and beginning of the root hair zone). Moreover, we found that the fungus preferentially infects immature root cells that are sensitive to these secreted fungal molecules, whereas infection is blocked in mature and insensitive parts of the root. Our study sheds light on novel and important features of the biology of this pathogen, which could contribute to its fitness in the rhizosphere.