Three Apodemus species occur in the Alps: the Alpine specialist A. alpicola, the generalist A. sylvaticus, and A. flavicollis. Based on molecular phylogeny, these species are closely related, with A. alpicola and A. flavicollis being sister species. The three species are extremely difficult to identify based on morphological characters, thus constituting cryptic species. The present study addressed the relationship between their habitat preferences and the morphological differentiation of their masticatory apparatus, on the small geographical scale of the Massif des Écrins in the French Alps. A geometric morphometric analysis of mandible and molar shape was implemented, complemented by an analysis of biomechanical ratios describing mandible functioning. Regarding the habitats, A. flavicollis appeared as restricted to humid forest lowlands, while A. alpicola occupies a wide range of high-altitude habitats; A. sylvaticus appears as a generalist species which habitat largely overlaps those of the two other species. From a morphological point of view, A. alpicola appeared well differentiated from both, A. sylvaticus and A. flavicollis, regarding molar shape, mandible size and shape. This morphological divergence presumably involves an adaptive response to a diet enriched in invertebrate preys, requiring an elongated incisor, but not so powerful chewing. In contrast, the two forest dwellers A. sylvaticus and A. flavicollis appeared extremely close in their morphology, hindering any robust identification based on molar or mandible morphology. Intraspecific variation of mandible morphology along the altitudinal gradient is also documented for both, the highly generalist A. sylvaticus, and the high-altitude specialist A. alpicola, suggesting ability to adjust to local resources on a short-time scale. Given the current global warming, deeply affecting Alpine environments, this ability to respond to changing resources may be crucial for the mid-term survival of the Alpine specialist A. alpicola.