The cosmopolitan genus Hedysarum L. (Fabaceae) is divided into sections Hedysarum, Stracheya, and Multicaulia. This genus includes many valuable medicinal, melliferous, and forage species. The species taxonomy and genome relationships within the sections are still unclear. We examined intra- and interspecific diversity in the section (sect.) Hedysarum based on repeatome analyses using NGS data, bioinformatic technologies, and chromosome FISH mapping of 35S rDNA, 5S rDNA, and the identified satellite DNA families (satDNAs). A comparison of repeatomes of H. alpinum, H. theinum, and H. flavescens revealed differences in their composition. However, similarity in sequences of most satDNAs indicated a close relationship between genomes within sect. Hedysarum. New effective satDNA chromosomal markers were detected, which is important for karyotype analyses within Hedysarum. Intra- and interspecific variability in the chromosomal distribution patterns of the studied markers were revealed, and species karyograms were constructed. These results provided new insight into the karyotype structures and genomic diversity within sect. Hedysarum, clarified the systematic position of H. sachalinense and H. arcticum, and confirmed the distant genomic relationships between species from sections Hedysarum and Multicaulia. Our findings are important for further comparative genome studies within the genus Hedysarum.