Fungus-animal symbioses have evolved countless times across the tree of life. While the stability of these mutualistic or parasitic interkingdom interactions often depends on optimized nutrient exchange, we lack a framework to explore whether animal-derived nutrients are optimal for fungal symbionts. We propose that this conceptual gap has constrained studies of how fungus-animal symbioses achieve ecological success as well as predictions about whether they will remain evolutionarily stable over time. We use Nutritional Geometry (NG) to harness nutritional niche theory and identify the crucial fundamental and realized nutritional niche dimensions of fungi that mediate symbiotic stability. We hypothesize that the dimensions of fungal nutritional niches are governed by their symbiotic role (mutualist vs. pathogen), degree of animal host control over nutritional competition (monoculture vs. polyculture), and breadth of host associations (specialist vs. generalist). We then show how these NG predictions can be rigorously tested integrating cleverly designed NG experiments with recent technological advances. We propose that this general theory can provide powerful niche-based insights into phenomena ranging from coevolutionary arms races to the potential emergence of economically important pathogens.