How do animals regulate self-movement despite large variation in the luminance contrast of the environment? Insects are capable of regulating flight speed based on the velocity of image motion, but the mechanisms for this are unclear. The Hassenstein–Reichardt correlator model and elaborations can accurately predict responses of motion detecting neurons under many conditions but fail to explain the apparent lack of spatial pattern and contrast dependence observed in freely flying bees and flies. To investigate this apparent discrepancy, we recorded intracellularly from horizontal-sensitive (HS) motion detecting neurons in the hoverfly while displaying moving images of natural environments. Contrary to results obtained with grating patterns, we show these neurons encode the velocity of natural images largely independently of the particular image used despite a threefold range of contrast. This invariance in response to natural images is observed in both strongly and minimally motion-adapted neurons but is sensitive to artificial manipulations in contrast. Current models of these cells account for some, but not all, of the observed insensitivity to image contrast. We conclude that fly visual processing may be matched to commonalities between natural scenes, enabling accurate estimates of velocity largely independent of the particular scene.