Many animals have the potential to discriminate colors absent from the rainbow: the non-spectral colors. Purple is the only such color for humans. It is perceived when two color cone-types in the retina (blue and red), with non-adjacent spectral sensitivity curves, are simultaneously stimulated. Purple is considered non-spectral because no monochromatic light (such as from a rainbow) can cause this simultaneous stimulation. Except in primates and bees, few behavioral experiments have directly examined non-spectral color discrimination, and little is known about non-spectral color perception in animals with more than three types of color photoreceptor. Birds have four color cone-types (compared to three in humans) and might perceive additional non-spectral colors such as ultraviolet+red and ultraviolet+green. Can birds discriminate non-spectral colors, and are these colors behaviorally and ecologically relevant? Here, using comprehensive behavioral experiments, we show that wild hummingbirds can discriminate a variety of non-spectral colors. We also show that hummingbirds, relative to humans, likely perceive a far greater proportion of natural colors as non-spectral. Our analysis of a large database of plumage and plant spectra reveals many colors that would be perceived as non-spectral by birds but not humans: birds’ extra cone-type allows them not just to see ultraviolet light but also to discriminate additional non-spectral colors. Our results support the idea that birds have tetrachromatic color vision and indicate that non-spectral color perception is vital for signaling and foraging. Since tetrachromacy appears to have evolved early in vertebrates, this capacity for rich non-spectral color perception is likely widespread.