Behavior can provide useful traits for testing phylogenetic hypotheses, and some details of orb web construction behavior have been especially useful in characterizing higher-level groups in spiders. The cues used to guide construction behavior and behavioral responses to these cues hold similar promise, but have never been used in phylogenetic studies. Here we use several techniques to test the hypothesis that orb webs in the two major branches of orb-weaving araneomorph spiders (Araneoidea and Deinopoidea) are monophyletic, using both the cues that guide orb construction and the spiders’ responses to these cues. If orb webs evolved only once, the expectation is that these traits should be similar in members of both evolutionary lines. This prediction was supported: species in the two groups use several of the same cues, and respond to them in similar ways. These cues include two identical reference stimuli for positioning sticky spiral lines; supplies of silk available in their glands that affect the positioning of sticky spiral loops; and at least one stimulus related to the size of the available space for the orb, which is used to trigger similar modifications of seven independent orb design traits. Neither group used tension-related cues to guide sticky spiral placement. These comparisons reinforce previous conclusions supporting orb web monophyly that were derived from morphological, molecular, and behavioral traits.