The establishment of coral microbial communities in early developmental stages is fundamental to coral fitness, but its drivers are largely unknown, particularly for bacteria. Using an in situ reciprocal transplant experiment, we examined the influence of parents and both the planulation and early recruit environment on the microbiome of offspring in the brooding coral Pocillopora damicornis. ITS2 rDNA and 16S rRNA gene metabarcoding showed that bacterial and microalgal endosymbiont communities varied according to parental and planulation environments, but not with early recruit environment. Microalgal communities of recruits were highly similar to those of their respective parents, but also contained additional low abundance strains, suggesting both vertical transmission and novel (‘horizontal’) acquisition. Such mixed mode transmission was also suggested for bacteria, although compelling evidence for vertical transmission was found for only one strain. Altogether, recruits harboured more diverse and variable microbiomes compared to their parents, indicating winnowing occurs as corals mature.