The microbiomes of host organisms and their direct source environments are closely linked and key for shaping microbial community dynamics. The relationship between these linked dynamics is largely unexplored because source substrates are usually unavailable. To address this current knowledge gap, we employed bacteriovorous nematodes as a unique model system, for which source substrates like rotting apples can be easily collected. We compared single host microbiomes with their corresponding apple source substrates, as well as nematode-free substrates, over a 2-year sampling period in the botanical garden in Kiel, Germany. We found that single worms have unique microbiomes, which overlap most strongly with nematodes from the same source apple. A comparison to previous, related work revealed that variation in microbiome composition of natural isolates is significantly influenced by the substrate type, from which worms were obtained (e.g., fruits or compost). Our current sampling further showed that microbiome assembly is mostly driven by dispersal limitation. Importantly, two independent analysis approaches consistently suggest that worm microbiomes significantly influence characteristics of the apple microbiomes, possibly indicating niche construction by nematodes. Moreover, combining apple microbiome and metabolome data, we identified individual microbes and specific compounds indicative of fruit ripening that are significantly associated with nematode presence. In conclusion, our study elucidates the complex relationship between host microbiomes and their directly connected substrate microbiomes. Our analyses underscore the significant influence of nematode microbiomes on shaping the apple microbiome and, consequently, the fruit's metabolic capacity, thereby enhancing our general understanding of host-microbiome interactions in their natural habitat.IMPORTANCEAlmost all complex organisms are host to a microbial community, the microbiome. This microbiome can influence diverse host functions, such as food processing, protection against parasites, or development. The relationship between host and microbiome critically depends on the assembly of the microbial community, which may be shaped by microbes in the directly linked environment, the source microbiome. This assembly process is often not well understood because of the unavailability of source substrates. Here, we used nematodes as a model system that facilitates a direct comparison of host and source microbiomes. Based on a 2-year sampling period, we identified (i) a clear link between assembly dynamics of host and source microbiomes, (ii) a significant influence of nematode microbiomes on apple microbiomes, and (iii) specific microbes and compounds that are associated with the presence of nematodes in the sampled substrates. Overall, our study enhances our understanding of microbiome assembly dynamics and resulting functions.