The microbiota associated to xerophyte is a “black box” that might include microbes involved in plant adaptation to the extreme conditions that characterize their habitat, like water shortage. In this work, we studied the bacterial communities inhabiting the root system of Argania spinosa L. Skeels, a tree of high economic value and ecological relevance in Northern Africa. Illumina 16S rRNA gene sequencing and cultivation techniques were applied to unravel the bacterial microbiota’s structure in environmental niches associated to argan plants (i.e., root endosphere, rhizosphere, root-surrounding soil), not associated to the plant (i.e., bulk soil), and indirectly influenced by the plant being partially composed by its leafy residue and the associated microbes (i.e., residuesphere). Illumina dataset indicated that the root system portions of A. spinosa hosted different bacterial communities according to their degree of association with the plant, enriching for taxa typical of the plant microbiome. Similar alpha- and beta-diversity trends were observed for the total microbiota and its cultivable fraction, which included 371 isolates. In particular, the residuesphere was the niche with the highest bacterial diversity. The Plant Growth Promotion (PGP) potential of 219 isolates was investigated in vitro, assessing several traits related to biofertilization and biocontrol, besides the production of exopolysaccharides. Most of the multivalent isolates showing the higher PGP score were identified in the residuesphere, suggesting it as a habitat that favor their proliferation. We hypothesized that these bacteria can contribute, in partnership with the argan root system, to the litter effect played by this tree in its native arid lands.