Background Neurobiological measures may inform our understanding of individual differences in adolescents’ general risk for and resilience to depressive symptoms, including during the COVID-19 pandemic. We tested a developmental model linking variation in amygdala–subgenual anterior cingulate cortex (sgACC) resting-state connectivity to perceived parenting experiences earlier in adolescence, to concurrent depressive symptoms before the pandemic, and to subsequent depressive symptoms during the pandemic. Methods We used data from a longitudinal study that included three waves (N = 214 adolescents; ages 9–15 years at time 1 [T1], 11–17 years at T2, and 12–19 years during the pandemic at T3). We assessed positive parenting (warm and supportive) (T1), depressive symptoms (T1 to T3), and functional connectivity between the sgACC and basolateral (BLA) and centromedial amygdala (T1 and T2). We modeled associations among earlier positive parenting, amygdala–sgACC connectivity, and depressive symptoms before and during the pandemic. Results Less positive parenting at T1 was associated prospectively with stronger BLA–sgACC connectivity at T2 (β = −0.22) over and above the effect of BLA–sgACC connectivity at T1. Stronger BLA–sgACC connectivity, in turn, was associated with heightened depressive symptoms, both before the pandemic (r = 0.21) and during the pandemic (β = 0.19; independent of the effect of pre-pandemic symptoms). Conclusions Adolescents who experience less positive parenting may develop a pattern of BLA–sgACC connectivity that increases their risk for mental health problems. BLA–sgACC connectivity may be associated with depressive symptoms in general, including during periods of heightened risk for adolescents, such as the pandemic.