I may be wrong in assuming this but MOST agents have your best interest, it's how they generate more business by making sure you have a good experience.

They supposedly generate state-compliant rental agreements.

But I'll have to put around $27,000 down, to generate 300-400 a month, or about $4500/year.

If they are busy with Sales, which generate big commissions for them, they may not have the availability or focus that you desire, even if they have a big "team".

Time to get over the PTSD of a once in a generation market crash. 

This is extremely common here because there is almost never a Will involved, and typically, there are two or more generations of potential heirs to run down and deal with.

Also, the $250k price was chosen so that the property would generate cash flow for the wife based on $2k rent/mo. 

Legitimate self-employment activity or active business that generates "earned" income and absence of full time employees - that is how someone can qualify for a Solo 401k plan, you don't have to have an entity. 

Frankly, if you're not willing to fully flesh out the automation of STR tenants and tussle with AirBNB, VRBO, etc. policies (or worse, use those platforms as lead generation and have your own STR booking system), make your exit strategy to be a small local portfolio that won't expand for passive income or simply get an attractive portfolio enough to sell to a big corp like Sonder (who has bought small businesses before).

You have a great way to generate income with this business.