*The outcome of plant-microbe interactions is determined by a fine-tuned molecular interplay between the two partners. Little is currently known about the molecular dialogue between plant roots and filamentous pathogens. We describe here a new pathosystem for the analysis of molecular mechanisms occurring during the establishment of a compatible interaction between Arabidopsis thaliana roots and a root-infecting oomycete. *We performed cytological and genetic analyses of root infection during the compatible interaction between A. thaliana and Phytophthora parasitica. *Phytophthora parasitica uses appressoria to penetrate A. thaliana roots. Initial biotrophic growth is accompanied by the formation of haustoria, and is followed by a necrotrophic lifestyle. Arabidopsis thaliana mutants with impaired salicylic acid (SA), jasmonic acid (JA) or ethylene (ET) signaling pathways are more susceptible than the wild-type to infection. The salicylate- and jasmonate-dependent signaling pathways are concertedly activated when P. parasitica penetrates the roots, but are downregulated during invasive growth, when ethylene-mediated signaling predominates. *Thus, defense responses in A. thaliana roots are triggered immediately on contact with P. parasitica. Our findings suggest that the pattern of early defense mechanism activation differs between roots and leaves.