The vaginal microbiome is typically dominated by Lactobacillus species, whereas a shift toward a diverse anaerobe-rich community is associated with adverse reproductive outcomes, including bacterial vaginosis (BV). Although metronidazole suppresses BV-associated taxa, recurrence is common, highlighting the need for strategies that durably reinforce Lactobacillus crispatus dominance. Prebiotic approaches have been proposed, but head-to-head selectivity across vaginal taxa has not been systematically evaluated. To identify selective carbon sources, we screened 246 distinct carbohydrates across nine representative vaginal bacterial species and integrated these phenotypic data with a comparative genomic analysis of carbohydrate-active enzymes. This approach identified β-glucosides as a conserved and selective metabolic pathway in vaginal Lactobacillus crispatus. β-glucoside utilization is broadly conserved across vaginal L. crispatus strains yet deficient in many BV-associated taxa, including Gardnerella, Prevotella, Fannyhessea vaginae, and Lactobacillus iners. In contrast, utilization genes of previously proposed raffinose-class oligosaccharides demonstrate reduced conservation among vaginal lactobacilli. In monoculture assays, β-glucoside substrates robustly support growth across diverse L. crispatus isolates while failing to support the growth of BV-associated organisms. Published studies further indicate that common fungal pathogens such as Candida albicans and Candida glabrata have limited capacity to utilize β-linked glucosides, suggesting a reduced risk of off-target fungal expansion. In a defined vaginal community in vitro model, selective substrates reproducibly shift community composition toward L. crispatus dominance. In vitro enrichment remains compatible with antibiotic treatment and in the presence of multiple endogenous sugars. Together, these findings support selective carbon utilization as a targeted strategy to reinforce L. crispatus within vaginal communities.