The melanized yeast Exophiala dermatitidis is resistant to many environmental stresses and is used as a model for understanding the diverse roles of melanin in fungi. Here, we describe the extent of resistance of E. dermatitidis to acute γ-radiation exposure and the major mechanisms it uses to recover from this stress. We find that melanin does not protect E. dermatitidis from γ-radiation. Instead, environmental factors such as nutrient availability, culture age and culture density are much greater determinants of cell survival after exposure. We also observe a dramatic transcriptomic response to γ-radiation that mobilizes pathways involved in morphological development, protein degradation and DNA repair, and is unaffected by the presence of melanin. Together, these results suggest that the ability of E. dermatitidis to survive γ-radiation exposure is determined by the prior and the current metabolic state of the cells as well as DNA repair mechanisms, and that small changes in these conditions can lead to large effects in radiation resistance, which should be taken into account when understanding how diverse fungi recover from this unique stress.