With shifts in island area, isolation, and cycles of island fusion-fission, the role of Quaternary sea-level oscillations as drivers of diversification is complex and not well understood. Here, we conduct parallel comparisons of population and species divergence between two island areas of equivalent size that have been affected differently by sea-level oscillations, with the aim to understand the micro- and macroevolutionary dynamics associated with sea-level change. Using genome-wide datasets for a clade of seven Amphiacusta ground cricket species endemic to the Puerto Rico Bank (PRB), we found consistently deeper interspecific divergences and higher population differentiation across the unfragmented Western PRB, in comparison to the currently fragmented Eastern PRB that has experienced extreme changes in island area and connectivity during the Quaternary. We evaluate alternative hypotheses related to the microevolutionary processes (population splitting, extinction, and merging) that regulate the frequency of completed speciation across the PRB. Our results suggest that under certain combinations of archipelago characteristics and taxon traits, the repeated changes in island area and connectivity may create an opposite effect to the hypothesized "species pump" action of oscillating sea levels. Our study highlights how a microevolutionary perspective can complement current macroecological work on the Quaternary dynamics of island biodiversity.