Festuca rubra subsp. pruinosa is a perennial grass that inhabits sea cliffs of the Atlantic coasts of Europe. In this unhospitable environment plants grow in rock crevices and are exposed to abiotic stress factors such as low nutrient availability, wind, and salinity. Festuca rubra subsp. pruinosa is a host of the fungal endophyte Epichloë festucae, which colonizes aerial organs, but its root mycobiota is unknown. The culturable endophytic mycobiota of FRP roots was surveyed in a set of 105 plants sampled at five populations in marine cliffs from the northern coast of Spain. In total, 135 different fungal taxa were identified, 17 of them occurred in more than 10% of plants and in two or more populations. Seven taxa belonging to Fusarium, Diaporthe, Helotiales, Drechslera, Slopeiomyces, and Penicillium appeared to be constituents of the core microbiome of Festuca rubra subsp. pruinosa roots because they occurred in more than 20% of the plants analyzed, and at three or more populations. Most fungal strains analyzed (71.8%) were halotolerant. The presence of Epichloë festucae in aboveground tissue was detected in 65.7% of the plants, but its presence did not seem to significantly affect the structure of the core or other root microbiota, when compared to that of plants free of this endophyte. When plants of the grass Lolium perenne were inoculated with fungal strains obtained from Festuca rubra subsp. pruinosa roots, a Diaporthe strain significantly promoted leaf biomass production under normal and saline (200 mM NaCl) watering regimes. These results suggest that the core mycobiome of Festuca rubra subsp. pruinosa could have a role in host plant adaptation, and might be useful for the improvement of agricultural grasses.