Intraspecific trait variation, including animal personalities and behavioural syndromes, affects how individual animals and populations interact with their environment. Within-species behavioural variation is widespread across animal taxa, which has substantial and unexplored implications for the ecological and evolutionary processes of animals. Accordingly, we sought to investigate individual behavioural characteristics in several populations of a desert-dwelling fish, the Australian desert goby (Chlamydogobius eremius). We reared first generation offspring in a common garden to compare non-ontogenic divergence in behavioural phenotypes between genetically interconnected populations from contrasting habitats (isolated groundwater springs versus hydrologically variable river waterholes). Despite the genetic connectedness of populations, fish had divergent bold-exploratory traits associated with their source habitat. This demonstrates divergence in risk-taking traits as a rapid phenotypic response to ecological pressures in arid aquatic habitats: neophilia may be suppressed by increased predation pressure and elevated by high intraspecific competition. Correlations between personality traits also differed between spring and river fish. River populations showed correlations between dispersal and novel environment behaviours, revealing an adaptive behavioural syndrome (related to dispersal and exploration) that was not found in spring populations. This illustrates the adaptive significance of heritable behavioural variation within and between populations, and their importance to animals persisting across contrasting habitats.