Shelled pteropods are marine planktonic snails that are regarded as bioindicators of ocean acidification because their thin aragonitic shells are susceptible to dissolution. In addition, shelled pteropods play an important role in the ocean’s carbonate budget and in marine food webs worldwide, despite their small body size. It is unclear if pteropod species are genetically homogeneous across their broad spatial ranges, or composed of several distinct species or populations. Little is also known about their evolutionary potential to adapt to long-term environmental changes. I aimed to assess the spatial genetic variation in the shelled pteropod Limacina bulimoides, to gain insight into the drivers of genetic structuring in the open ocean and to obtain a better understanding of their evolutionary history and adaptive potential. Through standard barcoding genes and novel target capture probes for pteropods, I investigated the patterns of genome-wide variation of L. bulimoides across their interconnected subtropical and tropical ocean habitat. I found that L. bulimoides is not genetically homogeneous across its range, but is composed of at least three reproductively isolated lineages across the Atlantic, Indian and Pacific Oceans. Detailed analysis of the Atlantic lineage revealed three distinct populations separated by narrow dispersal barriers, which suggests that (bio-)physical factors, natural selection, or a combination of both could be keeping populations apart. Looking forward, the methods used to access genomic information in L. bulimoides can be applied to other shelled pteropods, including species in (sub)polar regions, which are already experiencing the effects of a rapidly acidifying ocean.