ABSTRACT It is unknown how the human and rodent auditory cortices develop distinct communication processing capabilities. Decoding auditory signals is a challenging task due to the fleeting nature of the auditory scene. From humans to mice, one strategy believed to be important in decoding auditory signals is distributing the computational load between the left and right Auditory Cortices (i.e., lateralization). The circuitry underlying these sound-processing tasks is most receptive to refinement during critical periods when the brain is shaped by neural activity reflecting sensory information in the current environment. We hypothesize that asynchronous timing of critical periods between hemispheres may serve as a key mechanism underlying the development of functional specializations. To investigate, we compared measures of thalamocortical and intracortical maturation that have been previously associated with critical periods in sensory cortices. Our findings revealed that the transition from immature to mature patterning in thalamocortical activation of the left auditory cortex lags behind that of the right auditory cortex. Additionally, indicators of inhibitory and excitatory synapse development showed earlier maturation in the right auditory cortex. To evaluate the functional relevance of this asynchronous maturation between the auditory cortices, we manipulated the acoustic environment of male and female juvenile mice and tested the impact on tonotopic map re-arrangement in adulthood. Notably, tone rearing male mice resulted in tone overrepresentation in the right Auditory Cortex, while tone rearing within the same time window led to the opposite trend in females, with overrepresentation in the left auditory cortex. These findings suggest that differential timing in hemisphere development could precipitate lateralized auditory functioning in a sex-specific manner. Using spatial transcriptomics, we aim to uncover the molecular pathways that may coordinate asynchronous maturation between the hemispheres and how they are disrupted in neuropsychiatric disorders.