Plants engage in symbiotic relationships with soil microorganisms to overcome nutrient limitations in their environment. Among the best studied endosymbiotic interactions in plants are those with arbuscular mycorrhizal (AM) fungi and N-fixing bacteria called rhizobia. The mechanisms regulating plant nutrient homeostasis and acquisition involve small mobile molecules such as peptides and micro RNAs (miRNAs). A large number of CLE (CLAVATA3/EMBRYO SURROUNDING REGION-RELATED) and CEP (C-TERMINALLY ENCODED PEPTIDE) peptide hormones as well as certain miRNAs have been reported to differentially respond to the availability of essential nutrients such as nitrogen (N) and phosphorus (P). Interestingly, a partially overlapping pool of these molecules is involved in plant responses to root colonization by rhizobia and AM fungi, as well as mineral nutrition. The crosstalk between root endosymbiosis and nutrient availability has been subject of intense investigations, and new insights in locally or systemically mobile molecules in nutrient- as well as symbiosis-related signaling continue to arise. Focusing on the key roles of peptides and miRNAs, we review the mechanisms that shape plant responses to nutrient limitation and regulate the establishment of symbiotic associations with beneficial soil microorganisms.