Candida albicans is a fungus that colonizes the gut, oral, and vaginal mucosae of most humans without causing disease. However, under certain predisposing conditions this fungus can cause disease. C. albicans has several factors and attributes that facilitate its commensal and pathogenic lifestyles including the transition from a yeast to a hyphal morphology, which is accompanied by the expression of virulence factors. These factors are central in candidiasis that can range from invasive to superficial. This review focusses on one example of a superficial disease, i.e. vulvovaginal candidiasis (VVC) that affects approximately 75% of women at least once with some experiencing four or more symptomatic infections per year (RVVC). During VVC, fungal factors trigger inflammation, which is maintained by a dysregulated innate immune response. This in turn leads to immunopathology and symptoms. Another unique characteristic of the vaginal niche, is its Lactobacillus-dominated microbiota with low species diversity that is believed to antagonize C. albicans pathogenicity. The importance of the interactions between C. albicans, the host, and vaginal microbiota during commensalism and (R)VVC is discussed in this review, which also addresses the application of this knowledge to identify novel treatment strategies and to study vaginal C. albicans infections.