To better define the sweetpotato polyploidy, we sought to reconstruct phylogenies of its subgenomes based on hybridization networks that could trace reticulate lineages of differentiated homoeolog triplets of multiple single-copy genes. In search of such homoeolog triplets, we distinguished cDNA variants of 811 single-copy Conserved Ortholog Set II (COSII) genes from two sweetpotato clones into variation partitions specified by corresponding homologs from two I. trifida lines, I. tenuissima and I. littoralis using a phylogenetic partition method, and amplicon variants of the COSII-marker regions from 729 of these genes from two sweetpotato clones into putative homoeoallele groups using haplotype tree and the partition methods referenced by corresponding homologs from I. tenuissima. These analyses revealed partly or completely differentiated expressed-homoeologs and homoeologs from a majority of these genes with three important features. 1. Two variation types: the predominant interspecific variations (homoeoalleles), which are non-randomly clustered, differentially interspecifically conserved or sweetpotato-specific, and the minor intraspecific ones (alleles), which are randomly distributed mostly at non-interspecifically variable sites, and usually sweetpotato-specific. 2. A clear differentiation of cDNA variants of many COSII genes into the variation partition specified by I. tenuissima or I. littoralis from that by I. trifida. 3. Three species-homolog-specified and one sweetpotato-specific variation partitions among 293 different COSII cDNAs, and two or three out of the four partitions among cDNA variants of 306 COSII genes. We then constructed hybridization networks from two concatenations of 16 and 4 alignments of 8 homologous COSII cDNA regions each, which included three taxa of expressed homoeologs in a triple-partition combination from the 16 or 4 sweetpotato COSII genes and 5 taxa each of respective cDNA homologs from the three sweetpotato relatives and I. nil, and inferred a species tree embodying both networks. The species tree predicted close-relative origins of three partly differentiated sweetpotato subgenomes.