SummaryBiocrusts are phototroph‐driven communities inhabiting arid soil surfaces. Like plants, most photoautotrophs (largely cyanobacteria) in biocrusts are thought to exchange fixed carbon for essential nutrients like nitrogen with cyanosphere bacteria. Here, we aim to compare beneficial interactions in rhizosphere and cyanosphere environments, including finding growth‐promoting strains for hosts from both environments.To examine this, we performed a retrospective analysis of 16S rRNA gene sequencing datasets, host–microbe co‐culture experiments between biocrust communities/biocrust isolates and a model grass (Brachypodium distachyon) or a dominant biocrust cyanobacterium (Microcoleus vaginatus), and metabolomic analysis.All 18 microbial phyla in the cyanosphere were also present in the rhizosphere, with additional 17 phyla uniquely found in the rhizosphere. The biocrust microbes promoted the growth of the model grass, and three biocrust isolates (Boseasp._L1B56,Pseudarthrobactersp._L1D14 andPseudarthrobacter picheli_L1D33) significantly promoted the growth of both hosts. Moreover, pantothenic acid was produced byPseudarthrobactersp._L1D14 when grown onB.distachyonexudates, and supplementation of plant growth medium with this metabolite increasedB.distachyonbiomass by over 60%.These findings suggest that cyanobacteria and other diverse photoautotrophic hosts can be a source for new plant growth‐promoting microbes and metabolites.