The green-brown polymorphism in Orthoptera is a prominent example of the coexistence of multiple colour variants, especially since this polymorphism is shared by many species. The processes that maintain phenotypic polymorphisms depend on the underlying genetic and developmental regulation of body colouration, but these are not well understood for Orthoptera. Here we report on the inheritance of the green-brown polymorphism in the meadow grasshopper Pseudochorthippus parallelus, a species with four discrete colour morphs that differ in the distribution of green colouration across the body. We provide the most detailed analysis of the green-brown polymorphism to date using half-sib full-sib breeding and phenotyping of 4,300 offspring. The data strongly support a simple Mendelian control of the presence/absence of green colour in different regions of the body, involving four autosomal loci, two of which are genetically linked. However, estimation of population allele and haplotype frequencies using probabilistic simulations shows weak linkage disequilibrium in the population. The contrast between pedigree and population linkage suggests the presence of long-standing allelic variation and thus corroborates that long-term balancing selection is acting. Our study confirms and extends our understanding of inheritance patterns within the Chorthippus clade, providing unprecedented insights into the number and linkage of loci involved. The results have implications for the maintenance of polymorphisms and suggest that fluctuations in the phenotypic composition of populations can be generated by the segregation of genetic variants even in the absence of fluctuating selection.