Research on the neural imprint of dual-language experience, crucial for understanding how the brain processes the first (L1) and second language (L2), remains inconclusive. Conflicting evidence suggests either similarity or distinction in neural processing, with implications for bilingual patients with brain tumors. Preserving dual-language functions after surgery requires considering pre-diagnosis neuroplastic changes. Here, we combine univariate and multivariate fMRI methodologies to test a group of healthy Spanish-Basque bilinguals and a group of bilingual patients with gliomas affecting the language-dominant hemisphere while they overtly produced sentences in either their L1 or L2. Findings from healthy participants revealed the presence of a shared neural system for L1 and L2, while also identifying regions with distinct language-dependent activation and lateralization patterns. Specifically, while the L1 engaged a more left-lateralized network, L2 production relied on the recruitment of a bilateral basal ganglia-thalamo-cortical circuit. Notably, based on language lateralization patterns, we were able to robustly decode (AUC: 0.86 ± 0.18) the language being used. Conversely, bilingual patients exhibited bilateral activation patterns in both their L1 and L2. For the L1, regions such as the cerebellum, thalamus, and caudate acted in concert with the sparsely activated language-specific nodes. In the case of L2, the recruitment of the default mode network was notably prominent. These results demonstrate the compensatory engagement of non-language-specific networks in the preservation of bilingual speech production, even in the face of pathological conditions. Overall, our findings underscore the pervasive impact of dual-language experience on brain functional (re)organization, both in health and disease.