Preheat oven to 400 degrees F (200 degrees C). Grease a 9x13-inch baking dish lightly with cooking spray.
Heat olive oil in a large skillet over medium heat. Cook and stir onion and garlic until slightly softened, 3 to 5 minutes. Add summer squash; cook and stir until almost tender, 3 to 5 minutes. Stir in half of the green chile peppers, 1 teaspoon chili powder, and 1/4 teaspoon pepper; cook for 1 minute. Remove from heat.
Melt butter in a saucepan over medium heat. Stir in remaining 1 teaspoon chili powder, flour, salt, and 1/8 teaspoon pepper; cook for 1 minute. Pour in milk and stir until sauce thickens, about 5 minutes. Remove from heat. Stir in 1 cup Monterey Jack cheese; add remaining green chile peppers.
Stir 1/2 cup sauce into the squash mixture. Spoon 1/3 cup of the squash and sauce mixture into the center of each tortilla; roll up.
Arrange filled tortillas in the baking dish. Cover with remaining sauce. Cover baking dish with aluminum foil.
Bake in the preheated oven until heated through, about 25 minutes. Top with remaining 1/2 cup Monterey Jack cheese and tomatoes.