1. The significance of host–microbe interactions is increasingly appreciated across biological disciplines, yet to what extent these interactions influence developmental outcomes within and across generations remains poorly understood.

2. This study investigated the putative role of host–microbe interactions in the adaptive diversification of Onthophagus dung beetles, one of the most species‐rich and ecologically successful genera of insects. Onthophagus mothers vertically transmit growth‐ and fitness‐enhancing gut symbionts to their offspring through a faecal secretion known as the pedestal.

3. Pedestals were reciprocally exchanged between two ecologically similar congeneric Onthophagus species to assess the degree to which pedestal microbiota from one species can substitute for those of another.

4. It was found that the presence of a heterospecific pedestal delays development and increases mortality, and that the fitness costs of non‐host‐specific microbiota are maintained transgenerationally.

5. Collectively, these results support the hypothesis that Onthophagus beetles maintain, interact with, and are dependent upon host species‐specific microbial communities to support normal growth and development. The implications of these results are discussed in the context of host microbiota coevolution.