During colonization of the human nasopharynx, multiple strains of the Gram-positive pathogen Streptococcus pneumoniae coexist and compete with each other using secreted antimicrobial peptides called bacteriocins. The major class of pneumococcal bacteriocins is encoded by the blp operon, whose transcription is controlled by the secretion and detection of a polymorphic family of quorum sensing (QS) peptides. We examined interactions between the blp QS signal (BlpC) and receptor (BlpH) across 4,096 pneumococcal genomes. Imperfect genomic concordance between nine QS signal peptides and five phylogenetically-related QS receptor groups suggested extensive signal crosstalk (where cells produce signals that non-clonal cells detect) and eavesdropping (where cells respond to signals that they do not produce). To test this, we quantified the response of reporter strains containing one of six different blp QS receptors to cognate and non-cognate synthetic peptide signals. As predicted, we found evidence for eavesdropping in four of these receptors and for crosstalk in five of six tested signals. These in vitro results were confirmed during interactions between adjacent pneumococcal colonies, providing evidence that crosstalk and eavesdropping occur at endogenous, ecologically-relevant, levels of signal secretion. Using a spatially explicit stochastic model, we show that eavesdropping genotypes gain evolutionary advantages during inter-strain competition, even when their affinity to non-cognate signals is as low as 10% of the affinity to their cognate signal. Our results highlight the importance of social interactions in mediating intraspecific competition among bacteria and clarify that diverse competitive interactions can be mediated by polymorphism in QS systems.