Animals exist in intimate symbiotic partnerships with bacteria, often inherited by progeny from their parent early in development. This vertical transmission helps to promote strong fidelity and specificity of beneficial symbionts between generations, which may be compromised if there is colonisation from environmental bacteria later in the life cycle. Like many marine invertebrates, the sponge Amphimedon queenslandica has a biphasic life cycle that involves a pelagic larva settling and metamorphosing on the benthos. The complete morphological remodelling at that time makes the postlarval sponge susceptible to colonisation by environmental bacteria, which could challenge the fidelity of the inherited microbiome. To test this hypothesis, we combine long-read 16S rRNA gene amplicon sequencing with fluorescent microscopy to assess relative abundance and spatial distribution of inherited and environmentally-derived bacteria in embryos, swimming larvae, settled post-larvae and juveniles. We reveal highly dynamic and nuanced temporal changes in taxonomic composition of the microbiome before and after settlement, but these do not appear to affect the abundance or spatial localisation of the dominant inherited symbionts. Our study thus suggests that the fidelity of the vertically-inherited symbionts is not compromised, indicating deterministic regulation by the holobiont to ensure maintenance of a functionally specific microbiome across generations.