Actinobacteria are abundant in soil and well-known for producing antimicrobial compounds. Increasingly, members of this phylum are also found to form symbiotic relationships, for example with plants and insects, and provide protection against host infection. However, it remains poorly understood how Actinobacteria can be selectively recruited to the host microbiome from the environment. Acromyrmex echinatior leafcutter ants transmit Pseudonocardia bacteria between generations and also recruit Streptomyces species to their cuticular microbiome. RNA Stable Isotope Probing (SIP) experiments demonstrated that ants supply carbon-based resources to their cuticular bacteria. In turn, RNA-sequencing showed that genes encoding Pseudonocardia secondary metabolites, including bacteriocins and terpenes, were expressed in vivo on the ant cuticle. This suggests that publicly available host resources fuel interference competition between microbial species on the cuticle, which in turn selects for antibiotic-producing bacteria. In addition to leafcutter ants, Actinobacteria are known to be abundant in plant roots. Several plant-growth-promoting and antibiotic-producing Streptomyces bacteria were isolated from the root microbiome of Arabidopsis thaliana. Root exudates are hypothesised to play a major role in root microbiome assembly and DNA SIP, coupled with Illumina sequencing showed that these were utilised by many bacterial genera. However, Streptomyces appeared to be outcompeted for resources by fast-growing Proteobacteria, despite the fact that streptomycete isolates could grow on purified root exudates in the absence of competition. We found no evidence that the plant defense phytohormone salicylic acid selectively recruits Streptomyces to the plant root microbiome, which contradicts the conclusions made by previous published studies and suggests that they make use of other resources. Overall, this research demonstrates that host-nutrients, coupled with priority effects, can help to define competitive outcomes within the host microbiome. Understanding factors that influence the establishment of protective bacteria has implications for the development of more consistent biocontrol strategies.