GRIN disorders are rare neurodevelopmental disorders caused by pathogenic variants in the GRIN genes that encode the N-methyl-D-aspartate receptor (NMDAR) subunits. Two such missense variants of the GluN1 subunit, GRIN1-G620R and GRIN1-G827R, have been identified in multiple patients with profound intellectual disability and developmental delay. To understand the nature of the NMDAR deficits imparted by these variants, we generated Grin1 G620R and G827R mouse models that mimic the heterozygous condition found in affected individuals. Synaptic function was assessed using electrophysiological recordings made from the CA1 region of hippocampal slices prepared from adult knock-in mice of both sexes and their wild-type littermate counterparts. Interestingly, we found no change in basal AMPA receptor (AMPAR)-mediated transmission in G620R mice, whereas G827R mice exhibited a modest increase in AMPAR-mediated response that was associated with reduced paired-pulse facilitation. In contrast, NMDAR-dependent synaptic transmission and long-term potentiation were substantially diminished in both G620R and G827R mice, although greater deficits were observed for the G827R variant. Western blot analysis of surface GluN1 protein revealed that while synaptic NMDAR expression levels were unchanged in G620R mice, they were reduced in G827R mice. Together, these results suggest that both the GRIN1 G620R and G827R variants cause a substantial loss of synaptic NMDAR function, but via distinct mechanisms. Namely, our data indicate that GluN1-G620R subunits are likely incorporated into synaptic NMDARs where they serve to reduce channel function, whereas GluN1-G827R subunits are likely to have assembly or trafficking changes that result in a reduced expression of NMDARs at the synapse.