Traits contributing to the competence of biocontrol bacteria to colonize plant roots are often induced in the rhizosphere in response to plant components. However, pathogenic or beneficial fungi colonizing roots create a different niche that influences bacterial behavior. Such combined effects of root and associated fungus on rhizobacterium gene expression were investigated here with the help of the biocontrol bacterium Pseudomonas fluorescens Pf29Arp influenced by the wheat roots colonized by the take-all fungus Gaeumannomyces graminisvar. tritici (Ggt). Bacteria were inoculated on healthy, early Ggt-colonized and necrotic roots and transcriptomes were compared by shotgun DNA microarrays. Pf29Arp decreased disease severity when inoculated before the onset of necrosis. Necrotic roots exerted a broader effect on gene expression compared to early Ggt-colonized and healthy roots. A gene encoding a putative T6SS component was only induced under necrotic condition. A common pool of Pf29Arp genes differentially expressed on Ggt-colonized roots was related to carbon metabolism and oxidative stress, with a highest fold change with necrosis. Overall, the data shows that the association of the pathogenic fungus with the roots strongly altered Pf29Arp adaptation with differences between early and late Ggt infection steps.