To explore how social networks might respond to ecological change we investigated the impact of two natural resource pulses at the foraging and nidic levels on intra- and inter-specific territorial behaviour of two species that co-occur year-round in multi-species groups. We simulated conspecific and heterospecific territorial intrusions in two insectivorous cavity-nesting species using 974 model presentations with territorial song playbacks during and after a dual resource pulse of insect (bark beetle) prey and nest cavities across 5 years in British Columbia, Canada. As beetle abundance increased, both species increased aggression toward conspecific intruders, but at peak beetle abundance, the (typically) subordinate generalist insectivore, mountain chickadee (Poecile gambeli), attacked model intruders more frequently than did the dominant bark insectivore, red-breasted nuthatch (Sitta canadensis). Surprisingly, chickadees shifted to an inter-specific resource defense strategy, responding more aggressively to nuthatch intruders than to conspecifics. Thus, obligate secondary cavity nesting chickadees dominated facultative excavating nuthatches, providing evidence of a dominance reversal at the nesting guild level. Both insectivores increased defense of high-quality territories, with increasing availability of food resources. The reversal in the interspecific dominance hierarchy suggests that behavioural mechanisms governing social networks and community structure may change during resource pulses. Overall, we suggest that social networks of chickadees and nuthatches are dynamic with high complexity and flexibility to major ecological disruptions. Future work that examines the fitness consequences of temporal variation in social network dynamics and resiliency could help to reveal evolutionary mechanisms by which these species co-exist.