Biological soil crusts (biocrusts) are communities of microbes that inhabit the surface of arid soils and provide essential services to dryland ecosystems. While resistant to extreme environmental conditions, biocrusts are susceptible to anthropogenic disturbances that can deprive ecosystems of these valuable services for decades. Until recently, many culture-based efforts to produce inoculum for cyanobacterial biocrust restoration in the Southwestern US focused on producing and inoculating the most abundant primary producers and biocrust pioneers, Microcoleus vaginatus and members of the family Coleofasciulaceae (previously the M. steenstrupii complex). The discovery that a unique microbial community characterized by diazotrophs is intimately associated with M. vaginatus, known as the “cyanosphere”, suggests a symbiotic division of labor in which nutrients are traded between phototroph and heterotrophs. To explore the role and potential of the cyanosphere community for development of biocrust, we performed targeted isolation of cyanosphere inhabitants and used co-cultivation with M. vaginatus and other pioneer cyanobacteria under nutrient poor conditions, in both laboratory and field conditions, to test for beneficial interactions. We found co-inoculation of soil substrates with cyanosphere constituents resulted in more rapid development of cyanobacterial biocrusts over inoculation with the cyanobacterium alone. Further, we found that adding only beneficial heterotrophs to moderately to highly disturbed native soils facilitated the formation of a cohesive biocrust from remnant biocrust communities, without need of additional phototrophic biomass. Our findings highlight the hitherto unknown role of beneficial heterotrophic bacteria in the establishment and growth of biocrusts and allow us to make recommendations of biocrust restoration efforts based on presence of remnant biocrust communities in disturbed areas. Future biocrust restoration efforts should consider cyanobacteria and their beneficial community to be the true pioneers. Therefore, the inclusion of cyanobacteria and their beneficial community is instrumental for rapid establishment of incipient biocrust, thus rapidly restoring ecosystem services.