Social touch, an important aspect of social interaction and communication, is essential to kinship across animal species. Although often perceived as pleasurable, social touch can become considered aversive under certain contexts and often in individuals with Autism Spectrum Disorders (ASD). However, little is known about the neural circuits that contribute to social touch aversion in ASD. Rodent models provide an opportunity to interrogates these circuits, but social touch has not been thoroughly investigated in rodents, in part due to the lack of appropriate assays. We designed a novel head-fixed assay for social touch in mice, in which the experimenter has complete control to elicit highly stereotyped bouts of social touch between two animals. The user determines the number, duration, context, and type of social touch interactions, while monitoring an array of complex, aversive behavioral responses with high resolution cameras. We validated this assay in two different models of autism spectrum disorder (ASD), the Fmr1 knockout (KO) model of Fragile X Syndrome and maternal immune activation mice. We observed higher rates of avoidance running, hyperarousal, and aversive facial expressions (AFEs) to social touch than to object touch, in both ASD models compared to controls. Because this new social touch assay for head-fixed mice can be used to record neural activity during repeated bouts of social touch, we assessed how social touch is encoded in the relevant vS1, tS and BLA circuits and how social touch encoding is perturbed in Fmr1 KO mice. We find that vS1 in wild type mice can distinguish social from non-social touch, thereby encoding differences in texture. tS activity reflects salience encoding, such that the firing of cells is driven more by social than object touch when touch is voluntary and vice-versa when touch is forced. Finally, activity in the BLA is only driven by touch that is strongly aversive (i.e. forced object touch). In Fmr1 KO mice, vS1 and tS activity are similarly modulated by social and object touch suggesting that these regions cannot discriminate between the two types of touch. The inability to distinguish between social and non-social touch is also reflected at the behavioral level in the FXS mouse model. Furthermore, Fmr1 KO mice have a similar proportion of cells responding to aversive behaviors during social and object across vS1, tS and BLA. These experiments shed light on how the inability of cortical, striatal and amygdalar circuits to distinguish social touch from aversive non-social touch may contribute to the emergence of social touch aversion in ASD mouse models.