Background: Colour polymorphic species provide invaluable insight into processes that generate and maintain intra-specific variation. Despite an increasing understanding of the genetic basis of discrete morphs, sources of colour variation within morphs remain poorly understood. Here we use the polymorphic tawny dragon lizard Ctenophorus decresii to test simple Mendelian models for the inheritance of discrete morphs, and to investigate the genetic basis of continuous variation among individuals across morphs. Males of this species express either orange, yellow, orange surrounded by yellow, or grey throats. Although four discrete morphs are recognised, the extent of orange and yellow varies greatly. We artificially elevated testosterone in F0 females and F1 juveniles to induce them to express the male throat colour polymorphism, and quantified colour variation across the pedigree. Results: Inheritance of discrete morphs in C. decresii best fit a model whereby two autosomal loci with complete dominance respectively determine the presence of orange and yellow. However, a single locus model with three co-dominant alleles for orange, yellow and grey could not be definitively rejected. Additionally, quantitative expression of the proportion of orange and yellow on the throat was strongly heritable (orange: h2 = 0.84 ± 0.14; yellow: h2 = 0.67 ± 0.19), with some evidence for covariance between the two. Conclusions: Our study supports the theoretical prediction that polymorphism should be governed by few genes of major effect, but implies broader genetic influence on variation in constituent morph traits.