An urgent problem of the role of Slavic expansion in shaping gene pools of the population of Europe is being analyzed actively using various methods to study ancient and current populations. However, it is difficult to solve due to the lack of consolidated data on the Y-haplogroups in Slavic-, Finnish-, and Turkic-speaking populations of European Russia. The study aimed to look into genetic portraits of Mordovian populations and Russians of the Ryazan Region relative to the surrounding populations of indigenous peoples of Central Russia. For the first time the Y-gene pool of the Volga–Oka region (10 populations, n = 1136 individuals) was assessed in a broad context of our own data on the gene pools of European Russia (based on a single panel of 35 Y-haplogroups, 80 populations, n = 9712). The analysis was performed by multidimensional scaling (MDS) and computed cartography (GeneGeo). The produced series of 35 maps of the Y-gene pool of Central Russia and maps of genetic distances from peoples of the Volga–Oka region describe the gene-geographic landscape of the region in detail. It has been shown that all the assessed Russian populations belong to the common “Slavic” cluster that also includes representatives of Western Slavs. The cluster of populations of the Ural–Volga region including three Finnish-speaking populations of Mordovia (Erzya, Moksha, Shoksha) and 7 Turkic-speaking populations of the Chuvash and Mishar turned out to be the most genetically close to the Russian populations of Central Russia. It has been hypothesized that this group of populations can be traced back to the gene pool of the ancient indigenous Finnish-speaking population of the Volga–Oka region.