Abstract Although the mechanisms driving genome size evolution have not yet been fully deciphered, one potentially important factor is the dynamic of accumulation in mobile selfish genetic elements named transposable elements (TEs). Because the majority of these sequences are neutral or slightly deleterious, a negative correlation between genome size and selection efficacy is expected. Nevertheless, previous studies relying on empirical data from closely related species have yielded inconsistent conclusions, leaving this matter contentious. Here, we reconstructed a phylogeny based on whole genome data (2,242 genes) for 82 lineages representing 77 Drosophilid species. We studied correlations between genome size, TE content and measures of selection efficacy. We highlighted a strong phylogenetic inertia on genome size, and confirmed that TEs are the major components of the genome size. Using an integrative approach controlling for shared history, we found genome-wide ratios of non-synonymous over synonymous divergence ( dN/dS ) to be strongly positively correlated to genome size and TE content, especially in GC poor genes. This work provides evidence for TE proliferation in the genome of flies when purifying selection is reduced and the genetic drift is increased. In the end, this study emphasizes the critical importance of controlling for GC heterogeneity when testing for the controversial correlation between evolutionary rates and genome size.