Age-related decrements in cognitive ability have been proposed to stem from deteriorating function of the hippocampus. Many birds are long lived, especially for their relatively small body mass and elevated metabolism, making them a unique model of resilience to aging. Nevertheless, little is known about avian age-related changes in cognition and hippocampal physiology. We studied spatial cognition and hippocampal expression of the age-related gene, Apolipoprotein D (ApoD), and the immediate early gene Egr-1 in zebra finches at various developmental time points. In a first experiment, middle-aged adult males outperformed middle-aged females in learning correct food locations in a four-arm maze, but all birds remembered the task equally well after a 5- or 10-day delay. In a second experiment comparing young and old birds, aged birds showed minimal evidence for deterioration in spatial cognition or motivation relative to young birds, except that aged females showed less rapid gains in accuracy during spatial learning than young females. These findings indicate that sex differences in hippocampus-dependent spatial learning and decline with age are phylogenetically conserved. With respect to hippocampal gene expression, adult females expressed Egr-1 at significantly greater levels than males after memory retrieval, perhaps reflecting a neurobiological compensation. Contrary to mammals, ApoD expression was elevated in young zebra finches compared with aged birds. This may explain the near absence of decrements in spatial memory due to age, possibly indicating an alternative mechanism of managing oxidative stress in aged birds.