Functional specialization and plasticity are fundamental organizing principles of the brain. Since the mid-1800s, certain cognitive functions have been known to be lateralized, but the provenance and flexibility of hemispheric specialization remain open questions. Language is a uniquely human phenomenon that requires a delicate balance between neural specialization and plasticity, and language learning offers the perfect window to study these principles in the human brain. In the current study, we conducted two separate functional MRI experiments with language learners (male and female), one cross-sectional and one longitudinal, involving distinct populations and languages, and examined hemispheric lateralization and learning-dependent plasticity of the following three language systems: reading, speech comprehension, and verbal production. A multipronged analytic approach revealed a highly consistent pattern of results across the two experiments, showing (1) that in both native and non-native languages, while language production was left lateralized, lateralization for language comprehension was highly variable across individuals; and (2) that with increasing non-native language proficiency, reading and speech comprehension displayed substantial changes in hemispheric dominance, with languages tending to lateralize to opposite hemispheres, while production showed negligible change and remained left lateralized. These convergent results shed light on the long-standing debate of neural organization of language by establishing robust principles of lateralization and plasticity of the main language systems. Findings further suggest involvement of the sensorimotor systems in language lateralization and its plasticity.