Diet affects the intestinal microbiota. Increasingly, research is linking the intestinal microbiota to various human health outcomes. Consumption of traditional prebiotics (inulin, fructo-oligosaccharides, and galacto-oligosaccharides) confers health benefits through substrate utilization by select intestinal microorganisms, namely Bifidobacterium and Lactobacilli spp. A similar but distinct concept focused on microorganisms to support human health is through direct consumption of certain live microorganisms recognized as probiotics, which classically include Lactobacilli or Bifidobacterium strains. With advances in sequencing technologies and culturing techniques, other novel functional intestinal microorganisms are being increasingly identified and studied to determine how they may underpin human health benefits. These novel microorganisms are targeted for enrichment within the autochthonous intestinal microbiota through dietary approaches and are also gaining interest as next-generation probiotics because of their purported beneficial properties. Thus, characterizing dietary approaches that nourish select microorganisms in situ is necessary to propel biotic-focused research forward. As such, we reviewed the literature to summarize findings on dietary approaches that nourish the human intestinal microbiota and benefit health to help fill the gap in knowledge on the connections between certain microorganisms, the metabolome, and host physiology. The overall objective of this systematic review was to summarize the impact of dietary interventions with the propensity to nourish certain intestinal bacteria, affect microbial metabolite concentrations, and support gastrointestinal, metabolic, and cognitive health in healthy adults. Findings from the 17 randomized controlled studies identified in this systematic review indicated that dietary interventions providing dietary fibers, phytonutrients, or unsaturated fatty acids differentially enriched Akkermansia, Bacteroides, Clostridium, Eubacterium, Faecalibacterium, Roseburia, and Ruminococcus species, with variable effects on microbial metabolites and subsequent associations with physiologic markers of gastrointestinal and metabolic health. These findings have implications for biotic-focused research on candidate prebiotic substrates as well as next-generation probiotics.