While a suite of approaches have been developed to describe the scale, rate and spatial structure of exchange among populations, a lack of mechanistic understanding will invariably compromise predictions of population-level responses to ecosystem modification. In this study, we measured the energetics and sustained swimming capacity of giant Australian cuttlefish <i>Sepia apama</i> and combined these data with information on the life-history strategy, behaviour and circulation patterns experienced by the species to predict scales of connectivity throughout parts of their range. The swimming capacity of adult and juvenile <i>S. apama</i> was poor compared to most other cephalopods, with most individuals incapable of maintaining swimming above 15 cm s<sup>-1</sup>. Our estimate of optimal swimming speed (6–7 cm s<sup>-1</sup>) and dispersal potential were consistent with the observed fine-scale population structure of the species. By comparing observed and predicted population connectivity, we identified several mechanisms that are likely to have driven fine-scale population structure in this species, which will assist in the interpretation of future population declines.