Rootstocks are crucial for the sustainability of the citrus industry worldwide. Diploid intergeneric Citrus × Poncirushybrids have contributed considerably to citrus rootstock improvement and their tetraploid (doubled-diploid) forms are important resources for the creation of a new generation of tetraploid rootstocks. To optimize the efficiency of tetraploid rootstock breeding strategies, more knowledge is required on inheritance in the allotetraploid genitors. A set of 159 new SNP markers that fully distinguish Poncirus trifoliata (L.) Raf. from Citrus species was developed from polymorphisms mined in GBS data and used to establish a genetic map of tetraploid citrumelo (C. × paradisi Macfad. × P. trifoliata) and to analyze the meiotic behavior of tetraploid citrumelo and citrandarin (C. reticulata Blanco × P. trifoliata). The tetraploid citrumelo genetic map was highly syntenic and collinear with the clementine reference genome. The apparent intergeneric recombination rate was strongly limited by high preferential chromosome pairing, resulting in intermediate inheritance with disomic tendency. Such inheritance, also observed in tetraploid citrandarin, results in the transmission by the diploid gametes of a high rate of intergeneric heterozygosity. It is therefore expected that a large part of the genetic value selected in the original diploid intergeneric rootstock is transmitted to the tetraploid sexual progenies.