The Black Queen Hypothesis (BQH) is a novel theory that explains how selection can lead to dependencies on co-occurring microbes for lost metabolic functions in free-living organisms. The hypothesis posits that gene loss can provide a selective advantage by conserving resources, provided the gene's function is dispensable. Many vital genetic functions are leaky, producing public goods that benefit the entire community. The BQH predicts that the loss of a costly, leaky function will be selectively favored at the individual level until the production of public goods is just sufficient to support the equilibrium community. This process generates "beneficiaries" with reduced genomic content that are dependent on "helpers." The BQH may explain the non-universality of prototrophy, stress resistance, and other cellular functions in the microbial world. The hypothesis is illustrated through examples such as the loss of catalase-peroxidase (katG) in *Prochlorococcus* and its dependence on heterotrophic microbes for hydrogen peroxide detoxification. The BQH also discusses the potential for "shooting the moon," where a species becomes a helper for one function and then for others, leading to a niche with high resource requirements and job security. The hypothesis provides a framework for understanding microbial community dynamics and the persistence of rare keystone organisms.The Black Queen Hypothesis (BQH) is a novel theory that explains how selection can lead to dependencies on co-occurring microbes for lost metabolic functions in free-living organisms. The hypothesis posits that gene loss can provide a selective advantage by conserving resources, provided the gene's function is dispensable. Many vital genetic functions are leaky, producing public goods that benefit the entire community. The BQH predicts that the loss of a costly, leaky function will be selectively favored at the individual level until the production of public goods is just sufficient to support the equilibrium community. This process generates "beneficiaries" with reduced genomic content that are dependent on "helpers." The BQH may explain the non-universality of prototrophy, stress resistance, and other cellular functions in the microbial world. The hypothesis is illustrated through examples such as the loss of catalase-peroxidase (katG) in *Prochlorococcus* and its dependence on heterotrophic microbes for hydrogen peroxide detoxification. The BQH also discusses the potential for "shooting the moon," where a species becomes a helper for one function and then for others, leading to a niche with high resource requirements and job security. The hypothesis provides a framework for understanding microbial community dynamics and the persistence of rare keystone organisms.