We report a linkage map for Apios americana and describe synteny with selected warm-season legumes. A translocation event in common bean and soybean is confirmed against Apios and Vigna species. Apios (Apios americana; "apios"), a tuberous perennial legume in the Phaseoleae tribe, was widely used as a food by Native Americans. Work in the last 40 years has led to several improved breeding lines. Aspects of the pollination biology (complex floral structure and tripping mechanism) have made controlled crosses difficult, and the previous reports indicated that the plant is likely primarily an outcrosser. We used a pseudo-testcross strategy to construct a genetic map specific to the maternal parent. The map was built using single-nucleotide polymorphism markers identified by comparing the expressed sequences of individuals in the mapping population against a de novo maternal reference transcriptome assembly. The apios map consists of 11 linkage groups and 1121 recombinationally distinct loci, covering ~ 938.6 cM. By sequencing the transcriptomes of all potential pollen parents, we were able to identify the probable pollen donors and to discover new aspects of the pollination biology in apios. No selfing was observed, but multiple pollen parents were seen within individual pods. Comparisons with genome sequences in other species in the Phaseoleae showed extended synteny for most apios linkage groups. This synteny supports the robustness of the map, and also sheds light on the history of the Phaseoleae, as apios is relatively early diverging in this tribe. We detected a translocation event that separates apios and two Vigna species from Phaseolus vulgaris and Glycine max. This apios mapping work provides a general protocol for sequencing-based construction of high-density linkage maps in outcrossing species with heterogeneous pollen parents.