Inference of phylogeny is currently based on the concatenation of many genes, a procedure that enables reducing the stochasticity associated with single gene phylogenies. All possible drawbacks of this approach are however not fully understood, particularly the among gene heterogeneity of the phylogenetic signal. I studied the distribution of phylogenetic signal in the model system Drosophila using two genome-scaled datasets. Although both datasets apparently resolve most of the relationships with high support when analysed at the nucleotide level, there are at least two types of among genes phylogenetic incongruences. First, the phylogenetic signal is not homogenously distributed among nuclear coding, mitochondrial coding, and non-coding genes, which robustly support competing topologies at some nodes, particularly close to tips. Second, the phylogenetic signal is not homogenously distributed among ontology classes, whereby nuclear genes involved with the metabolism tend to carry their own signal. Most, but not all of these incongruences, are due to substitutions at synonymous sites which I show being affected by different mutational pressures in different types of data. Counter intuitively, partitioning is not successful in alleviating these incongruences, which are instead revealed by using across-site heterogeneous model or by using a coalescent aware approach. These results advocate that extra care should be taken when interpreting high supports from the analysis of genome scaled phylogenies, and that signal associated with synonymous sites may be unreliable even at the genus level. Phylogenetic incongruences may be however extremely instructive in disentangling possible sources of systematic error, as well as in revealing peculiar aspects of species biology such as introgression or incomplete lineage sorting due to fast radiation.