Reported herein are seven cases of a histologically distinct oncocytic papillary renal cell carcinoma (OPRCC) with an inverted nuclear pattern. To define its prognostic significance, the clinicopathological features of OPRCC were compared to those of types 1 and 2 PRCC. The median age of the seven patients was 67 years. Grossly, tumors were well-circumscribed and small (1.2 cm ± 0.4 cm). Microscopically, the OPRCC were composed of well-developed thin papillae, lined with a single layer of cuboidal-to-columnar oncocytic cells. The tumor cells had round-to-oval nuclei and eosinophilic granular cytoplasm, which was strongly positive for anti-mitochondrial immunostaining. The nuclei were characteristically polarized toward the surface of the papillae and contained mostly small nucleoli. The tumors had high expression of α-methylacyl-coenzyme A racemase, CD15, CD117, cytokeratin (CK) 7, E-cadherin, epithelial membrane antigen, MOC 31, mucin-1, vascular endothelial growth factor and vimentin, low expression of CD10 and Ki-67, and no expression of CK20. Genetically, gain of chromosomes 3p, 11q, and 17q, and loss of chromosome 4q was observed. All seven patients were alive with no recurrence or metastasis at a mean follow-up time of 37.1 ± 23.7 months. In conclusion, OPRCC show unique pathological features with indolent clinical behavior and are more similar clinicopathologically to type 1 than to type 2 PRCC.