Historically the dominant trend in comparative brain and behavior research has emphasized the differences in cognition and its neural basis among species. In fact, the vertebrate forebrain shows a remarkable range of diversity and specialized adaptations. Probably the major morphological variation is that observed in the telencephalon of the actinopterygian fish, which undergoes a process of eversion during embryonic development, relative to the telencephalon of non-actinopterygians (for instance, amniotes), which develops by a process of evagination. These different developmental processes produce notable variation, mainly two solid telencephalic hemispheres separated by a unique ventricle in the actinopterygian radiation that contrasts with the hemispheres with internal ventricles in other groups. However, an increasing amount of evidence reveals that the forebrain of vertebrates, whether everted or evaginated, presents a common pattern of basic organization that supports highly conserved cognitive functions. We analyze here recent data indicating a close functional similarity between spatial cognition mechanisms in different groups of vertebrates, mammals, birds, reptiles, and teleost fish, and we show in addition that they rely on homologous neural mechanisms. Thus, recent functional and behavioral comparative evidence is added to the developmental and neuroanatomical data suggesting that the evolution of cognitive capabilities and their neural basis in vertebrates could have been more conservative than previously realized.