In previous work, we showed that peptides from endocytosed proteins containing the tyrosine YXXφ sorting motif are recognized by the μ2 subunit of AP‐2, the plasma membrane clathrin adaptor protein complex. This interaction is activated by phosphoinositide lipids that are phosphorylated at the D‐3 position of the inositol ring, and is also enhanced by the formation of clathrin–AP‐2 coats. Here, we describe the detection of a specific interaction between peptides containing a second sorting motif, the dileucine motif, and AP‐1, the clathrin adaptor complex responsible for sorting proteins at the trans‐Golgi network (TGN). Surprisingly, the site of dileucine binding is the β1 subunit, not μ1. A YXXφ‐containing peptide from a protein trafficked within the TGN does bind to μ1, however. Phosphatidylinositol 3, 4‐diphosphate and 3, 4, 5‐triphosphate did not activate the interaction between dileucine‐containing peptides and AP‐1 but instead inhibited it, and clathrin–AP‐1 coat formation did not alter the interaction. Thus, there are at least two physically separate binding sites for sorting signals on APs, which are also regulated independently.