Active canonical Wnt signaling results in recruitment of β‐catenin to DNA by TCF/LEF family members, leading to transcriptional activation of TCF target genes. However, additional transcription factors have been suggested to recruit β‐catenin and tether it to DNA. Here, we describe the genome‐wide pattern of β‐catenin DNA binding in murine intestinal epithelium, Wnt‐responsive colorectal cancer (CRC) cells and HEK293 embryonic kidney cells. We identify two classes of β‐catenin binding sites. The first class represents the majority of the DNA‐bound β‐catenin and co‐localizes with TCF4, the prominent TCF/LEF family member in these cells. The second class consists of β‐catenin binding sites that co‐localize with a minimal amount of TCF4. The latter consists of lower affinity β‐catenin binding events, does not drive transcription and often does not contain a consensus TCF binding motif. Surprisingly, a dominant‐negative form of TCF4 abrogates the β‐catenin/DNA interaction of both classes of binding sites, implying that the second class comprises low affinity TCF‐DNA complexes. Our results indicate that β‐catenin is tethered to chromatin overwhelmingly through the TCF/LEF transcription factors in these three systems.