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Summary Chloroplast Unusual Positioning 1 (CHUP1) plays an important role in the chloroplast avoidance and accumulation responses in mesophyll cells. In epidermal cells, prior research showed silencingCHUP1‐induced chloroplast stromules and amplified effector‐triggered immunity (ETI); however, the underlying mechanisms remain largely unknown.CHUP1 has a dual function in anchoring chloroplasts and recruiting chloroplast‐associated actin (cp‐actin) filaments for blue light‐induced movement. To determine which function is critical for ETI, we developed an approach to quantify chloroplast anchoring and movement in epidermal cells. Our data show that silencingNbCHUP1inNicotiana benthamianaplants increased epidermal chloroplast de‐anchoring and basal movement but did not fully disrupt blue light‐induced chloroplast movement.SilencingNbCHUP1auto‐activated epidermal chloroplast defense (ECD) responses including stromule formation, perinuclear chloroplast clustering, the epidermal chloroplast response (ECR), and the chloroplast reactive oxygen species (ROS), hydrogen peroxide (H₂O₂). These findings show chloroplast anchoring restricts a multifaceted ECD response.Our results also show that the accumulated chloroplastic H₂O₂inNbCHUP1‐silenced plants was not required for the increased basal epidermal chloroplast movement but was essential for increased stromules and enhanced ETI. This finding indicates that chloroplast de‐anchoring and H₂O₂play separate but essential roles during ETI.