Two wild diploid wheat species, Triticum monococcum ssp. aegilopoides (Link) Thell. and T. urartu Tumanian ex Gandilyan, are closely related, and respectively harbor the Am and A genomes. The A-genome donor of tetraploid and common wheat is T. urartu, and T. monococcum ssp. monococcum L. is the cultivated form derived from the wild einkorn wheat T. monococcum ssp. aegilopoides. At least two superior traits are present in T. monococcum ssp. aegilopoides for wheat breeding, and the spikes and grains are generally larger in T. monococcum ssp. aegilopoides than in T. urartu. Thus, T. monococcum ssp. aegilopoides is considered to be a useful genetic resource. Although the genome information of T. urartu has been updated, genome-wide molecular markers have not been sufficiently developed in the subspecies aegilopoides. Here, we performed RNA sequencing (RNA-seq) analysis of leaf transcripts to survey genome-wide polymorphisms such as single-nucleotide polymorphisms (SNPs) and insertions/deletions (indels) in 15 accessions of the two diploid wheat species. The detected SNPs and indels covered the entire chromosomes of these species, and the phylogenetic study based on the polymorphisms showed recent divergence between the two subspecies, aegilopoides and monococcum. The phylogenetic study also allowed to compare the genetic diversity among the two diploid wheat species, the D-genome species Aegilops tauschii Coss., and the U-genome species Ae. umbellulata Zhuk. The wild einkorn wheat had the larger genetic diversity than Ae. umbellulata, whereas the diversity was smaller than that in Ae. tauschii. Similar to the previous reports, the subspecies aegilopoides accessions were grouped into three lineages, and the cultivated einkorn wheat was originated from one of the lineages. Next, we tried to confirm the addition of the subspecies aegilopoides chromosomes in nascent allohexaploid lines with AABBAmAm genomes, which were produced through interspecific crossing between a durum wheat cultivar Langdon and the various subspecies aegilopoides accessions. Cleaved amplified polymorphic sequence (CAPS) markers were designed to distinguish SNPs between the A and Am genomes. Use of the CAPS markers enabled to construct linkage maps in a mapping population of the subspecies aegilopoides accessions. The constructed linkage map allowed to detect successfully QTLs for heading and flowering time. Thus, the SNP and indel data should facilitate further genetic studies in wild einkorn wheat.