Tesla Motors Inc., facing opposition from the owners of car dealerships, is now eligible to operate its own stores in Richmond, Va., the Virginia Department of Motor Vehicles commissioner ruled on Wednesday.

The decision is an important win for Tesla as it tries to expand sales locations ahead of the introduction next year of a lower-priced Model 3 sedan. Chief Executive Officer Elon Musk has said the $35,000 car will take Tesla’s production to 500,000 in 2018 from about 50,000 last year.

States...