A set of actinobacterial strains was isolated from the root nodules of Acacia gerrardii grown as part of an afforestation trial in the Khurais desert, Saudi Arabia. Among them, five clonal isolates could not be unambiguously assigned to any recognized type species, and two of them, designated AC027S T and AC027N, were selected as representatives for taxonomic characterization. Cells were Gram-stain-positive, aerobic, non-motile, non-spore-forming, with short rods to coccoid-like morphology. Growth occurred at 20–42 °C, pH 5.0–10.0 and in the presence of up to 3.0% (w/v) NaCl. The major whole-cell sugar was glucose, and the muramic acid residues of the peptidoglycan carried peptide subunits composed of alanine, glutamic acid and lysine. The predominant menaquinone was MK-9(H4). Major fatty acids were iso-C 15:0 and anteiso-C 15:0 , and the polar lipid profile included diphosphatidylglycerol, phosphatidylglycerols and several unidentified glycophospholipids, glycolipids, phospholipids and lipids. Phylogenetic analysis based on 16S rRNA gene sequences placed AC027S T and AC027N within the genus Promicromonospora . Whole-genome sequence-based phylogenomic reconstruction and relatedness indices confirmed that these G+C-rich strains (72%) are distinct from all described Promicromonospora species, with Promicromonospora soli NEAU-GS50 T as the closest described relative. Consistent with their nodule-associated niche, the strains were able to degrade and utilize plant-derived substrates, tolerate microaerophilic conditions and possessed genes for mobilizing essential metals, such as iron and molybdenum, suggesting a supportive role in the nodule microbial community and in sustaining rhizobial nitrogen fixation, as reflected in an enhanced nodulation by native rhizobia when inoculated in desert soil. Based on phenotypic, chemotaxonomic and genomic evidence, strains AC027S T and AC027N represent a novel species of the genus Promicromonospora , for which the name Promicromonospora noduliphila sp. nov. is proposed. The type strain is AC027S T (=KCTC 59476 ᵀ , =JCM 37759ᵀ).