<p>Proteins undergo phase separation to form membraneless condensates that spatially organize biomolecular interactions. These condensates can support cellular physiology or instigate pathological protein aggregation. Tau and α-synuclein (αSyn) are neuronal proteins that form heterotypic Tau:αSyn condensates associated with physiological and pathological processes. Tau and αSyn regulate microtubules, but also misfold and co-deposit in aggregates linked to neurodegenerative disease, highlighting the ambivalent impact of Tau:αSyn condensation in health and disease. Here, we show that Tubulin modulates Tau:αSyn condensates by promoting microtubule interactions and inhibiting homotypic and heterotypic pathological oligomers. In the absence of Tubulin, Tau-driven condensation accelerates formation of pathogenic Tau:αSyn heterodimers and amyloid fibrils. Tubulin partitioning into condensates promotes microtubule polymerization and prevents Tau and αSyn oligomerization. We identify distinct Tau and αSyn structural states in pathological Tubulin-absent versus physiological Tubulin-rich condensates. In neuronal models, microtubule loss drives pathological oligomer formation and neurite loss, whereas inducible Tau condensation stabilizes microtubules.</p>