However, when you factor in the HELOC, we have a negative / break-even cash flow (HELOC payments are about 25% of the revenue from both).

Again several factors at play but just providing information based on your criteria.

They're good to have open access to capital/cash/equity to a property ahead of time so you can execute a deal or purchase when the time comes on a split second decision (versus having to apply to a loan at that time which might take 20-45 days to get approved/closed/etc plus by that time you dont know what your future income/credit/assets will be like in order to qualify anyway).The second use is sleep at night factor and having a reserve of capital in the event an emergency event occurs in life.For these two reasons is why I use lines of credit.

It's normally the desire for immediate income that steers most investors towards bad investments because they are hyper focused on cash flow which is often portrayed differently in spreadsheets than in real life, and should be a consideration but not deciding factor.

I successfully run 1 STR and have a 2nd that an inherited PM handles.I have Vrbo and Airbnb they will sync with each other with no external software.I set pricing easily by using the built in tools that Vrbo provides.Automated messages are built into both platforms.Vrbo keeps my calendar slammed, but I take direct bookings as needed, simple to do.I have no additional 3rd party fees to very sucessfuly run and manage my property needing only a a few minutes per week.

When you say the agent is not "running the comps correctly," what specific factors might they be overlooking that I should pay attention to?

It can be multiple factors. 

That can be the determining factor on if you have a good buyers agent. 

For a 2 bedroom my projected ongoing is around 13-15k (not counting the rent) at the end of the year because this is my first Airbnb Arbitrage I have and will make mistakes expense wise, the start up costs also is not factored because furnishing and starting everything from scratch obviously will skew the ongoing expenses which would add another 5-8k but I played it smart and have most of the funding charged to buisness credit cards with 0% APR for 12-18 months such that I save money and can take the year in paying back also with sign on bonuses which will save me up to 1.2k or more.If and when I hit my conservative projections my profit should be around 16,300-22000 by the end of the year this is after rent, expenses, cleaning fees and so on. 

That's a factor to consider if you have children and want them to be in a good school district.