Birds rapidly integrate visual information during flight and recent studies have revealed some of the fundamental algorithms for avian visual guidance. During hovering flight, hummingbirds respond to global visual motion (optic flow) in six major axes with essentially equal strength. In contrast, during forward flight hummingbirds respond to vertical but not lateral optic flow. Lateral position during forward flight is primarily controlled by balancing the left/right rate of image expansion. Hummingbirds also have two centers of acute vision (lateral vs. frontal). These findings raise the question of whether regions of the visual field contribute equally to guiding locomotion. To address this question, we measured 3D position and velocity during free flight in a tunnel for seven male Anna’s hummingbirds. Across seven experiments, we varied lateral and/or frontal optic flow or rate of image expansion by projecting specific patterns on the tunnel walls. When presented with vertical stripes moving either forward or backward on the sides, birds tended to reduce forward velocity, with forward motion yielding a stronger reduction. By presenting birds with a stationary, looming, or receding spiral in front, we found that forward velocity can be influenced by frontal optic flow, and more strongly by receding stimuli. Frontal expansion patterns had little effect on forward velocity. Moreover, we found that flight altitude was influenced by horizontal upward motion, but only when this motion was presented laterally or both laterally and frontally. Frontal motion alone had little effect on vertical course control. Collectively, these results suggest a relative importance of lateral cues over frontal in controlling both speed and altitude of hummingbird flight.