The present study focused on three autochthonous varieties of apple trees belonging to the old Tuscany germplasm (central Italy), Chitignano, Mora and Ruggine, and aimed to (a) evaluate the presence of the four main latent viruses of apple trees (apple chlorotic leaf spot virus [ACLSV], apple mosaic virus [ApMV], apple stem grooving virus [ASGV] and apple stem pitting virus [ASPV]) and (b) elucidate the biochemical and physiological responses of apple leaves and fruits challenged by ACLSV (the only virus detected). Indeed, despite no visible symptoms being reported, more than half of the assayed trees tested positive for ACLSV, although it occurred only in Mora and Ruggine. ACLSV impaired the photosynthetic performance of apple trees, especially in Ruggine leaves, but variety‐specific responses in terms of reorganization of photosynthetic pigment and primary metabolites were reported. Mora showed a higher ability to trigger the de‐epoxidation state of xanthophylls and to accumulate α‐tocopherol, while d‐glucose and sucrose increased only in infected Ruggine leaves, probably as a signalling response and/or an osmotic adjustment of this variety under ACLSV infection. Unexpectedly, ACLSV infection slightly increased pome size, but it dramatically reduced their quality (i.e., soluble solids content), again especially in Ruggine, the only variety where reductions of d‐fructose, d‐glucose and malic acid contents were reported. Overall, the evidence here reported could offer valuable insights to effectively cope with the detrimental viral diseases affecting this species and to protect the production of one of the most consumed and appreciated fruits in the world.