Dumpling squid, Euprymna tasmanica, show consistent individual differences in behaviour that can be classified according to indices reflecting shy–bold, activity and reactivity responses. Using crosses of wild-caught single males to multiple females with known behavioural phenotypes, this study estimated patterns of additive genetic and residual variance in these behavioural traits from offspring of squid in two contexts, a threat (antipredator) and feeding (foraging) test. Genetic contributions to behavioural expression were dependent on test context. Behaviours in antipredator contexts had significant heritabilities (h² = 0.2-0.8) while behaviours from foraging contexts had lesser additive genetic and greater residual components (h² = 0.05-0.08). Personality trait variation in females was not related to her fecundity. Female boldness in foraging situations, which co-varied with body size, explained small but significant variation ( 21%) in brood hatching success, while successful fertilization was determined by positive assortion of mate pairs according to their shy–bold phenotype. These results are discussed in terms of the ecological and evolutionary significance of animal 'personality' traits in wild populations of animals.