Mutualistic co-evolution can be mediated by vertical transmission of symbionts between host generations. Organisms exhibit adaptations that ensure optimal microbial inheritance, yet it is unknown if this extends to superorganismal social insects that host co-evolved gut microbiomes. Here, we document consistent vertical transmission that preserves more than 80 bacterial genera across colony generations in a fungus-farming termite model system. Inheritance is governed by reproductives, analogous to organismal gametes, that found new colonies and are endowed with environmentally-sensitive and termite-specific gut microbes. These symbionts are then reliably passed on within the offspring colony, where priority effects dictate the composition of the forming colony microbiome. Founding reproductives thus play a central role in transmission. However, in sharp contrast to organismal inheritance of an endosymbiont within an egg, the multicellular properties of the superorganismal gametes allow for inheritance of entire communities of co-adapted microbes. Superorganismal inheritance aligns the reproductive interests of the host colony and a diverse set of microbes and clarifies a fundamental driver of millions of years of termite-bacterial co-diversification. Ultimately, the high symbiotic fidelity and host control favors mutualistic cooperation that should surpass that of other animals with complex microbiomes.