Verticillium longisporum is a soil-borne fungal pathogen causing vascular disease predominantly in Brassicaceae. We have reported previously that the receptor of the plant defense hormone jasmonoyl-isoleucine (JA-Ile), CORONATINE INSENSITIVE 1 (COI1), is required in roots for efficient proliferation of the fungus in the shoot implicating a mobile root-borne signal that influences the outcome of the disease in shoots. This susceptibility-promoting COI1 function is independent from JA-Ile. To explore the underlying mechanism we compared the root transcriptome of coi1 with the transcriptomes of the susceptible JA-Ile-deficient allene oxide synthase (aos) mutant and susceptible wild-type (WT) plants. The biggest difference between the transcriptomes of coi1 versus WT and aos was due to 316 immunity-related genes that were constitutively higher expressed in coi1 as compared to the susceptible genotypes. Interfering with the expression of a subgroup of these genes partially suppressed the coi1-mediated tolerance phenotype. We therefore hypothesize that secreted defense compounds encoded by genes constitutively expressed in coi1 are transported to the shoot with the transpiration stream where they accumulate to interfere with fungal growth. We furthermore report that 149 of the 316 COI1-repressed genes are induced in WT and aos upon infection reaching similar levels as in mock-treated coi1. These were not further induced in coi1 upon infection. Thus, the repressive effect of COI1 is either lifted or overridden upon infection with V. longisporum.