Indigenous chickens represent a culturally significant and resilient resource in sustainable poultry production systems. Cricket powder (Acheta domesticus), recognized for its high-quality protein and environmentally friendly attributes, has emerged as a promising alternative protein source to enhance sustainability in poultry nutrition. This study investigated the biochemical and molecular responses to dietary cricket powder supplementation in three Thai indigenous chicken breeds: Betong KU line (BT), Nin Kaset black-meat with black feathers (NB), and Nin Kaset with white feathers (NW). A 15% inclusion of cricket powder in the diet was used to replace palm oil and partially substitute soybean meal, maintaining equivalent levels of crude protein and essential amino acids across diets. Cricket powder supplementation did not significantly affect physical meat quality traits such as pH, cooking loss, or Warner-Bratzler shear force. However, it notably enhanced soluble protein and collagen content, particularly in BT chickens. Moreover, significant increases in bioactive dipeptides—anserine and carnosine—were observed in NB chickens, indicating a breed-specific molecular response. These findings suggest that cricket powder supplementation can positively modulate muscle biochemistry and enhance bioactive compound profiles in Thai indigenous chickens, offering a sustainable strategy to improve meat functionality without compromising quality.