Apple replant disease (ARD) is a significant economic restraint to the successful re-establishment of new apple orchards on sites previously planted to the same crop. Pythium ultimum, an oomycete, is a significant component of the ARD pathogen complex. Although ethylene (ET)- and jasmonic acid (JA)-mediated defense responses are intensively studied in the foliar pathosystem, the transferability of this knowledge to the interaction between a perennial root system and soilborne pathogens is unknown. The aim of this study was to test the hypothesis that the ET/JA-mediated defense response is conserved in roots of tree crops in response to infection by P. ultimum. Apple genes with the annotated function of ET/JA biosynthesis, MdERF (ethylene response factor) for signaling transduction and a gene encoding a pathogenesis-related (PR) protein (β-chitinase, the target of ERF) were identified from the apple genome sequences. The transcriptional profiles of these genes during P. ultimum infection and after exogenous ET and/or JA treatment were characterized using qRT-PCR. Several genes showed a 10- to 60-fold upregulation in apple root tissue 24-48 h post inoculation (hpi). Exogenous ET and JA treatment exhibited either a positive or negative influence on expression of ET or JA biosynthesis genes, depending upon gene isoforms and the tissue types, while the expression of MdERF and the PR protein encoding gene was upregulated by both ET and JA treatment. Our data are consistent with the hypothesis that ET/JA-mediated defense pathways are functional in the root system of perennial tree species defending soilborne pathogens.