Species of the red algal genus Meristotheca are important natural resources that can be used directly as food for human consumption as well as raw materials for the extraction of carrageenan. Despite being harvested in Japan and Korea, a comprehensive taxonomic study of Meristotheca specimens from these two countries to elucidate their phylogenetic position is lacking. In this study, we aimed to clarify the taxonomic identities of specimens currently regarded as M. papulosa from Korea and Japan by analyzing morphological and molecular data. As the result, we recognized a new species, Meristotheca pilulaora sp. nov. from Korea and resurrected Meristotheca japonica for specimens from Japan. The two entities have long been identified as M. papulosa and exhibit similar external morphologies. They appeared independently in the concatenated phylogenetic tree of COI-5P and rbcL and could also be distinguished morphologically by the position of cystocarps (blade margins in M. pilulaora; marginal proliferations in M. japonica), spinose cystocarps (absent in M. pilulaora; present in M. japonica), and the number of cortical cell layers (two in M. pilulaora; 4–8 in M. japonica). The DNA analysis of M. pilulaora sp. nov. in local populations showed 11 COI-5P haplotypes on Jeju Island with no apparent geographical structure. High genetic diversity and occurrence of unique haplotypes in southern Jeju may provide a genetic basis for population with high thermal tolerance. These findings have strengthened our understanding of the species diversity of the genus Meristotheca and provided insights into conservation, management, and haplotype selection for the future cultivation of these economically important species.