The Due on Sale Clause was born out of Sub-To deals 30-40 years ago where properties are transferred to non-approved, usually unqualified applicants.

I'm a brand new, as green as you can get, have no idea what I'm doing or where to start investor.

The rates for a purchase money loan (one where you take the loan out to directly acquire the property) vs when you do a "cash out refinance", which your loan would be if you chose to pay off the line with a loan on the primary residence, it typically done at a higher rate.

Well, if you rolled it over to a Roth IRA where you manage it it might be better.But, if rates rise a little more, just pull from your retirement funds to cover. 

The minimum length that a vacation rental must be rented for depends on the zoning restrictions, which require either a thirty (30) day minimum rental or a one-week minimum rental, depending on where the property is located.

Potential locations for my first buy preferably somewhere close to where I reside (Virginia, Maryland, or North Carolina).

Where are you investing?

On the other hand these are also where you might find your deepest buys so it really just depends on your personal strategy and buy box, many investors are having success in these areas. 

What's the prevailing cap rate for similar assets/same class in the area where it's located?

There are a handful of ways where arbitrage ends with you running out of money.