1. Floral apparency is shaped by both mutualistic and antagonistic interactions that can act in opposing ways. Pollinators are expected to select for more visually apparent flowers, but this likely trades off against the potentially severe fitness costs of damage to apparent flowers by floral herbivores. One way in which flowers that close during parts of the day might circumvent this trade-off, is by evolving less visible lower petal surfaces that are inconspicuous to herbivores when flowers are closed. 2. Here we used visual system modelling and herbivory experiments to test whether petal surfaces that are exposed when flowers are closed are cryptically coloured. We collected lower and upper petal surface spectra for 77 Asteraceae species from Namaqualand, South Africa. This included closing species that expose their lower petal surfaces for 5 to 6 daylight hours, and non-closing species that do not expose their lower surfaces. We used these contrasting groups to test the expectation of reduced conspicuousness of lower petal surfaces in closing, but not non-closing species. 3. By modelling reflectance spectra of petal surfaces against a green leaf background in various visual systems we showed 1) that conspicuousness of upper petal surfaces to pollinators and various herbivores were strongly correlated, suggesting the potential for fitness trade-offs between attracting mutualists and antagonists to open flowers, 2) that closing species’ lower petal surfaces were less visible to herbivores against a leaf background than those of non-closing species, and 3) that closing species had larger differences between upper and lower petal surface colouration than non-closing species. Behavioural experiments with tortoise herbivores demonstrated that flowers are easily detected when upper surfaces are exposed, but that tortoises were unable to distinguish lower petal surfaces against a leaf background, resulting in reduced flower herbivory. 4. These results are consistent with selection by herbivores for cryptic colouration of lower petal surfaces, and divergence of colouration between lower and upper petal surfaces in species with closing flowers. Visual crypsis of flowers may be an effective anti-herbivory strategy during times when pollinators are inactive, and provides an alternative to chemical defence, which often involves costs to pollination.