Previous studies have shown that the basic properties of the visual representation of space are reflected in spatial language. This close relationship between linguistic and non-linguistic spatial systems has been observed both in typical development and in some developmental disorders. Here we provide novel evidence for structural parallels along with a degree of autonomy between these two systems among individuals with Autism Spectrum Disorder, a developmental disorder with uneven cognitive and linguistic profiles. In four experiments, we investigated language and memory for locations organized around an axis-based reference system. Crucially, we also recorded participants’ eye movements during the tasks in order to provide new insights into the online processes underlying spatial thinking. Twenty-three intellectually high-functioning individuals with autism (HFA) and 23 typically developing controls (TD), all native speakers of Norwegian matched on chronological age and cognitive abilities, participated in the studies. The results revealed a well-preserved axial reference system in HFA and weakness in the representation of direction within the axis, which was especially evident in spatial language. Performance on the non-linguistic tasks did not differ between HFA and control participants, and we observed clear structural parallels between spatial language and spatial representation in both groups. However, there were some subtle differences in the use of spatial language in HFA compared to TD, suggesting that despite the structural parallels, some aspects of spatial language in HFA deviated from the typical pattern. These findings provide novel insights into the prominence of the axial reference systems in non-linguistic spatial representations and spatial language, as well as the possibility that the two systems are, to some degree, autonomous.