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Although mutualisms are often studied as simple pairwise interactions, they typically involve complex networks of interacting species. How multiple mutualistic partners that provide the same service and compete for resources are maintained in mutualistic networks is an open question. We use a model bacterial community in which multiple ‘partner strains’ ofEscherichia colicompete for a carbon source and exchange resources with a ‘shared mutualist’ strain ofSalmonella enterica. In laboratory experiments, competingE. colistrains readily coexist in the presence ofS. enterica, despite differences in their competitive abilities. We use ecological modeling to demonstrate that a shared mutualist can create temporary resource niche partitioning by limiting growth rates, even if yield is set by a resource external to a mutualism. This mechanism can extend to maintain multiple competing partner species. Our results improve our understanding of complex mutualistic communities and aid efforts to design stable microbial communities.