Abstract Background The intertidal copepod Tigriopus californicus is a model for studying the process of genetic divergence in allopatry and for probing the nature of genetic changes that lead to reproductive isolation. Although previous studies have revealed a pattern of remarkably high levels of genetic divergence between the populations of this species at several spatial scales, it is not clear what types of historical processes are responsible. Particularly lacking are data that can yield insights into population history from the finest scales of geographic resolution. Results Sequence variation in both cytochrome b (CYTB, mtDNA) and the rieske iron-sulfur protein (RISP, nuclear) are examined at a fine scale within four different regions for populations of T. californicus. High levels of genetic divergence are seen for both genes at the broader scale, and genetic subdivision is apparent at nearly all scales in these populations for these two genes. Patterns of polymorphism and divergence in both CYTB and RISP suggest that selection may be leading to non-neutral evolution of these genes in several cases but a pervasive pattern of neither selection nor coadaptation is seen for these markers. Conclusion The use of sequence data at a fine-scale of resolution in this species has provided novel insights into the processes that have resulted in the accumulation of genetic divergence among populations. This divergence is likely to result from an interplay between a limited dispersal ability for this copepod and the temporal instability of copepod habitat. Both shorter-term processes such as the extinction/recolonization dynamics of copepod pools and longer-term processes such as geological uplift of coastline and sea level changes appear to have impacted the patterns of differentiation. Some patterns of sequence variation are consistent with selection acting upon the loci used in this study; however, it appears that most phylogeographic patterns are the result of history and not selection on these genes in this species.