The vagina hosts a rich microbiome that includes Candida albicans (Ca), a pathobiont that typically resides in a state of asymptomatic colonization. However, despite the high prevalence of vaginal carriage, our understanding of how Ca colonization shapes the host environment, and the vaginal microbiota is limited. Group B Streptococcus (GBS) is also a frequent colonizer of the vaginal tract and is associated with adverse pregnancy outcomes and neonatal invasive disease. We have developed a murine model of Ca-GBS co-colonization and find that Ca promotes GBS persistence and survival in the vagina, cervix, and uterus. To further our understanding, we performed transcriptomic analysis and identified key elements involved in interactions between Ca, GBS, and human vaginal epithelial cells. Notably, we find that Ca arginine biosynthesis is induced by GBS, which is directly implicated in bacterial fitness, virulence, and cytolytic activity. We have identified that expression of the arginine biosynthetic pathway by Ca contributes to GBS ascension from the vagina into the uterus. Moreover, we demonstrate that transcriptional reprogramming and direct binding between Ca and GBS promote bacterial fitness in the host environment. Future work will involve investigating mechanisms of interaction and the host innate immune response during co-colonization in vivo.