Roots of Arabidopsis thaliana do not engage in symbiotic association with mycorrhizal fungi but host taxonomically diverse fungal communities that influence health and disease states. We sequenced the genomes of 41 isolates representative of the A. thaliana root mycobiota for comparative analysis with 79 other plant-associated fungi. We report that root mycobiota members evolved from ancestors having diverse lifestyles and retained diverse repertoires of plant cell wall-degrading enzymes (PCWDEs) and effector-like small secreted proteins. We identified a set of 84 gene families predicting best endophytism, including families encoding PCWDEs acting on xylan (GH10) and cellulose (AA9). These genes also belong to a core transcriptional response induced by phylogenetically-distant mycobiota members in A. thaliana roots. Recolonization experiments with individual fungi indicated that strains with detrimental effects in mono-association with the host not only colonize roots more aggressively than those with beneficial activities but also dominate in natural root samples. We identified and validated the pectin degrading enzyme family PL1_7 as a key component linking aggressiveness of endophytic colonization to plant health. Overall design: We report the transcriptomes of six root mycobiota members in interaction in mono-association with their host Arabidopsis thaliana in gnotobiotic system. The six fungal strains used in this experiment were isolated from the roots of healthy Arabidopsis plants in the wild (Duran et al. 2018). To identify the genes they express in planta, we conducted a RNA-sequencing experiment. A. thaliana sterile seeds were inoculated with mycelium, then cultivated for 28 days on a phosphate-deficient agar-based medium. Roots were harvested and crushed, then total RNA was extracted and sequenced. As control conditions, mycelia were grown on the same plant culture medium and fungal RNA was extracted with the same method, after 28 days in culture. With this experiment, we identified a core set of genes - mostly composed of genes encoding carbohydrate active enzymes - which are over-expressed by all six fungi in the roots of A. thaliana. We believe they constitute a toolbox for root colonization and the endophytic lifestyle.