Heat 1 tablespoon of the olive oil in a skillet over medium heat. Add the minced garlic and chopped Vidalia onion and cook, stirring frequently, until the onions are soft and begin to brown (about 5 minutes).
Pour in the apple cider vinegar and stir to release the caramelized bits from the pan.
Transfer the onion mixture to a blender. Add the remaining olive oil, honey, Dijon mustard, salt, and pepper. Blend on high until smooth and emulsified. If the dressing is too thick, add a small amount more of oil and blend until you reach your desired consistency.
Mix in the poppy seeds and adjust the seasonings as needed. Pour the dressing into a clean container, cover, and refrigerate for at least 3 hours before serving.