A growing consensus favors the predominance of the human left hemisphere in manipulation and language (speech and gestures). However, the mechanisms underlying brain lateralization for noncommunication and communication functions are still unclear. Many studies emphasize the ambiguous nature of the relationship between the directions of brain lateralization for manipulation and for language. A comparative evolutionary approach investigating lateralization and communication mechanisms in our closest living relatives can improve our understanding of human hemispheric specialisation. We review theories concerning the evolutionary origins of human right-handedness and language and studies, highlighting the relevance of a comparative evolutionary approach. We discuss four methodological issues related to the study of handedness and communication: 1) categorisation of signaling based on criteria of intentionality; 2) use of a comprehensive multimodal and multifactorial approach; 3) investigation of laterality in intraspecific gestures; and 4) comparison of manual laterality between gestures and noncommunication actions. Deeper investigations of the multifaceted nature of intentionality in communication and the multidimensionality of manual laterality and communication in humans and other primates are needed. Finally, we make four recommendations to enhance our understanding of the evolutionary origins of human right-handedness and language: 1) implementing a comprehensive and integrated investigation of laterality and communication; 2) considering socioecologically relevant contexts; 3) investigating intraspecific aspects of communication in humans and other primates that vary in their degree of sociality; and 4) using appropriate, standardized methods of data collection and analysis.