A host of recent studies have reported robust representations of visual object information in the human parietal cortex, similar to those found in ventral visual cortex. In ventral visual cortex, both monkey neurophysiology and human fMRI studies showed that the neural representation of a pair of unrelated objects can be approximated by the averaged neural representation of the constituent objects shown in isolation. In this study, we examined whether such a linear relationship between objects exists for object representations in the human parietal cortex. Using fMRI and multivoxel pattern analysis, we examined object representations in human inferior and superior intraparietal sulcus, two parietal regions previously implicated in visual object selection and encoding, respectively. We also examined responses from the lateral occipital region, a ventral object processing area. We obtained fMRI response patterns to object pairs and their constituent objects shown in isolation while participants viewed these objects and performed a 1-back repetition detection task. By measuring fMRI response pattern correlations, we found that all three brain regions contained representations for both single object and object pairs. In the lateral occipital region, the representation for a pair of objects could be reliably approximated by the average representation of its constituent objects shown in isolation, replicating previous findings in ventral visual cortex. Such a simple linear relationship, however, was not observed in either parietal region examined. Nevertheless, when we equated the amount of task information present by examining responses from two pairs of objects, we found that representations for the average of two object pairs were indistinguishable in both parietal regions from the average of another two object pairs containing the same four component objects but with a different pairing of the objects (i.e., the average of AB and CD vs. that of AD and CB). Thus, when task information was held consistent, the same linear relationship may govern how multiple independent objects are represented in the human parietal cortex as it does in ventral visual cortex. These findings show that object and task representations coexist in the human parietal cortex and characterize one significant difference of how visual information may be represented in ventral visual and parietal regions.