Present-day phylogeographic patterns have been shaped by the dual histories of lineages and places, producing a diversity of relationships that may challenge discovery of general rules. For example, the predicted positive correlation between dispersal ability and gene flow has been supported inconsistently, suggesting unaccounted complexity in theory or the comparative framework. Here, I extend the sympatric sister-species approach, in which variance between lineages and places is minimized, to sister clades and test a fundamental assumption of comparative genetic studies of dispersal: that taxa which evolved at the same time and in the same place will, if they have similar life histories and ecologies, have essentially the same phylogeographic structure. Phylogenetic analyses of 197 Stigmatopora pipefishes using two nuclear (creatine kinase intron 6, α-tropomyosin) and two mitochondrial (16S, noncoding region) loci revealed largely synchronous parallel diversification of sister clades that are codistributed from Western Australia to New Zealand, supporting the null hypothesis. Only one comparison, however, yielded a sympatric sister-species pair (the two stem species), so I also explored the potential for extant species sharing a substantial proportion of their evolutionary histories in sympatry to substitute for sister taxon comparisons. In eastern Australia, where strong environmental structure is lacking, phylogeographic differences between species that have been codistributed for ∼85% of their evolutionary histories were consistent with tendencies favoured by their modest life-history differences, that is the larger, rarer species had lower genetic diversity. In contrast, in New Zealand, two species codistributed for ∼70% of their evolutionary histories were both structured similarly by a strong biogeographic filter despite differences in life history. Rigorously quantifying the influence of intrinsic and extrinsic factors on phylogeographic structure may advance most efficiently through meta-analyses of contemporaneously codistributed taxa, including but not limited to sympatric sister species.