Inverted repeats (IRs) are genetic elements with a DNA motif (left arm) followed by a gap, or spacer, and its reverse complement (right arm) – e.g., ATACGGnnnCCGTAT. They play a key role in manybiological functions, including gene regulation, DNA replication, and genome plasticity. In this study, we aim to systematically investigate the distribution of short IRs (with gap lengths up to 20 bp) in all completely sequenced prokaryotic species by confronting observed statistics to expected ones computed by permuting DNA sequences under specific constraints. Through this systematic approach, we reveal complex patterns of IR biases with five main observations: (i) a systematic enrichment of IRs with arm lengths longer than 6 bp, (ii) a systematic depletion of palindromes (IRs with a zero-length gap) shorter than 6 bp, (iii) qualitatively different biases between coding and non-coding regions, (iv) in non-coding regions, the most frequent enrichment over bacterial species occurs for gap length of 4 bp similar to the most common loop size of RNA hairpins associated with known transcription terminators in model organisms, and (v) biases in coding regions that strongly depend on the species considered. Altogether, these findings — both corroborating and further deepening previous analyses — highlight universal evolutionary constraints as well as species-specific selective pressures that act on genome sequences, particularly on IRs.