The hippocampal formation (HF) plays a crucial role in amniote spatial cognition. There are also indications of functional lateralization in the contribution of the left and right HF in processes that enable birds to navigate space. The experiments described in this study were designed to examine left and right HF differences in a task of sun compass-based spatial learning in homing pigeons (Columba livia). Control, left (HFL) and right (HFR) HF lesioned pigeons were trained in an outdoor arena to locate a food reward using their sun compass in the presence or absence of alternative feature cues. Subsequent to training, the pigeons were subjected to test sessions to determine if they learned to represent the goal location with their sun compass and the relative importance of the sun compass vs. feature cues. Under all test conditions, the control pigeons demonstrated preferential use of the sun compass in locating the goal. By contrast, the HFL pigeons demonstrated no ability to locate the goal by the sun compass but an ability to use the feature cues. The behaviour of the HFR pigeons demonstrated that an intact left HF is sufficient to support sun compass-based learning, but in conflict situations and in contrast to controls, they often relied on feature cues. In conclusion, only the left HF is capable of supporting sun compass-based learning. However, preferential use of the sun compass for learning requires an intact right HF. The data support the hypothesis that the left and right HF make different but complementary contributions toward avian spatial cognition.