Best to partner with a builder who has experience in JC and can navigate the permit/zoning process with the town plus do the renovation work needed.

I'm assuming things like taxes, permits, code, insurance etc.

All-in costs, including design, survey, permitting, construction loan interest, land, construction will be $360,000.

On the other hand, if the renovation is a true gut with plans and permits, you will need an architect.

If any permits were used, check to make sure they were signed off. 

My brother's rental is a little over 1,000s sqft heated living area, so the ADU would only be permitted for 500 sqft in Winston-Salem, according to information I found online .One advantage of an ADU I believe would be the ability to hook up to the primary residence's utilities. 

I was quoted $5,700 by licensed contractor and $3,200 by one not licensed who wouldn't pull a permit but has done several of these before.  

Other avenues to find contractors include: reviewing the neighborhood for signs of contractors already working in the neighborhoods that you are targeting, asking the town/borough for contractors that pull lots of permits (aka get hired a lot) in your area, as well as inquiring withe local Home Depot/Lowes early in the morning and seeing who is active.

I plan to go meet with the SLC Zoning/Permitting office to learn all I can, but thought I'd reach out here first. 

I have heard that Flagstaff has specific regulations for STRs, including licensing and permit requirements.