The gut microbiome is an important mediator of life-history traits in animals and performs essential functions that may allow hosts to exploit novel niches. However, sources of variation in microbiome abundance and composition within vertebrate species are poorly understood, particularly in wild birds. Here, we used 16S rRNA gene sequencing to describe the faecal microbiome of a trans-Saharan migratory passerine species breeding in Central Spain, the pied flycatcher (Ficedula hypoleuca), focusing on small-scale differences in bacterial composition and relative abundance between the natural habitat of the species (oakwood) and a newly created habitat (pinewood) located 1 km apart. We detected a difference in the composition of microbiomes of birds between the habitats, with birds from the oakwood showing a higher abundance of several bacterial taxa, such as Actinobacteriota and Proteobacteria. We observed no microbiome differences according to individual characteristics such as sex or age, although nestlings and females showed a higher abundance of certain bacteria, especially those in the oakwood habitat. We investigated metabolic pathways associated with the microbiome and detected a higher abundance of bacteria with fatty acid biosynthesis and degradation pathways and metabolite precursor and energy generation pathways in oakwood birds compared to pinewood birds. In the pinewood birds, we found a significant increase in bacteria with the L-alanine biosynthesis and pentose phosphate pathways. Our study improves our understanding of the gut microbiome composition of insectivore passerines and shows that local-scale environmental factors such as habitat are among the most important modulators of avian gut microbiome composition.