In some animals, offspring begging is elicited by parents through behavioural or morphological signals. The red spot on the lower mandible in adult gulls is one of the best-known examples of a signal triggering chick begging. We examined whether the begging response of chicks (pecking for food and the chatter call for drawing parental attention) was affected by the spot size within the natural range of variation on a dummy head. Using a cross-fostering experiment, we examined whether these responses covary with the size of the genetic or social parent's spot. We found that the natural variation in size of this parental signal strongly influenced intensity of chick begging. Pecking increased when chicks were stimulated by a larger red spot. Additionally, pecking intensity increased in chicks reared by mothers with a large red spot, suggesting that this begging component is influenced by previous experience. In contrast, chick hatching order affected the number of chatter calls produced in relation to the size of the red spot on the dummy, suggesting the presence of different begging strategies according to brood hierarchy. The differential call response to a small/large red spot on the dummy was positively correlated with the original mothers’ red spot size and negatively with that of the original fathers. These results suggest a genetic correlation between biased chick response for a large spot and parental signal in contrasting patterns for mothers and fathers. Our results suggest that the parental red spot and offspring begging are traits subject to coevolution.