The Arcuate Fasciculus (AF) is of considerable interdisciplinary interest, because of its major implication in language processing. Theories about language brain evolution are based on anatomical differences in the AF across primates. However, changing methodologies and nomenclatures have resulted in conflicting findings regarding interspecies AF differences: Historical knowledge about the AF originated from human blunt dissections and later from monkey tract-tracing studies. Contemporary tractography studies reinvestigate the fasciculus’ morphology, but remain heavily bound to unclear anatomical priors and methodological limitations. First, we aim to disentangle the influences of these three epistemological steps on existing AF conceptions, and to propose a contemporary model to guide future work. Second, considering the influence of various AF conceptions, we discuss four key evolutionary changes that propagated current views about language evolution: 1) frontal terminations, 2) temporal terminations, 3) greater Dorsal- versus Ventral Pathway expansion, 4) lateralisation. We conclude that new data point towards a more shared AF anatomy across primates than previously described. Language evolution theories should incorporate this more continuous AF evolution across primates.