Synapse degeneration contributes to cognitive decline in neurodegenerative diseases. We have previously demonstrated synaptic accumulation of pathological alpha-synuclein in synapses in brain tissue from people who died with Dementia with Lewy Bodies (DLB), but whether this occurs in Parkinson’s disease (PD), a related neurodegenerative synucleinopathy, remains unknown, as do mechanisms of synapse degeneration in these diseases. Oligomeric tau has been implicated in synaptotoxicity in tauopathies, including Alzheimer’s disease, and growing evidence supports that the co-aggregation of different pathological proteins may contribute to their toxicity. Here, we tested the hypothesis that oligomeric tau and phosphorylated alpha-synuclein co-aggregate in synapses, where they could contribute to synapse dysfunction and degeneration. We prepared synaptic enriched fractions from frozen human DLB (n=7), PD (n=5), and age and sex-matched control (n=7) brain tissue and found both alpha-synuclein and tau in synaptic fractions. We used tissue embedded for array tomography combined with two high-resolution microscopy techniques: array tomography and Förster resonance energy transfer (FRET), to examine synaptic localisation of pathological proteins in human DLB (n=7), PD (n=4), and age and sex-matched control (n=7) brain tissue. We observe that phosphorylated alpha-synuclein and oligomeric tau are present together within individual synapses where they generate a FRET signal. These data indicate that in both DLB and PD, pathological forms of alpha-synuclein and tau form hetero-oligomers within individual synaptic terminals, where they likely contribute to synaptic dysfunction and loss.