In addition to the normal set of standard (A) chromosomes, some eukaryote species harbor supernumerary (B) chromosomes. In most cases, B chromosomes show differential condensation with respect to A chromosomes and display dark C-bands of heterochromatin, and some of them are highly enriched in repetitive DNA. Here we perform a comprehensive NGS (next-generation sequencing) analysis of the repeatome in the grasshopper Abracris flavolineata aimed at uncovering the molecular composition and origin of its B chromosome. Our results have revealed that this B chromosome shows a DNA repeat content highly similar to the DNA repeat content observed for euchromatic (non-C-banded) regions of A chromosomes. Moreover, this B chromosome shows little enrichment for high-copy repeats, with only a few elements showing overabundance in B-carrying individuals compared to the 0B individuals. Consequently, the few satellite DNAs (satDNAs) mapping on the B chromosome were mostly restricted to its centromeric and telomeric regions, and they displayed much smaller bands than those observed on the A chromosomes. Our data support the intraspecific origin of the B chromosome from the longest autosome by misdivision, isochromosome formation, and additional restructuring, with accumulation of specific repeats in one or both B chromosome arms, yielding a submetacentric B. Finally, the absence of B-specific satDNAs, which are frequent in other species, along with its euchromatic nature, suggest that this B chromosome arose recently and might still be starting a heterochromatinization process. On this basis, it could be a good model to investigate the initial steps of B chromosome evolution.