Can I auto collapse the Custom Forms in the Project Details section on a project?

Are you maybe still in Classic? This functionality or similar is available in NWE but I don't think anything has been made available in Classic.

Mine collapse automatically. I kinda wish I could un-collapse them automatically :)

Oh I found it in the top right corner there is a little icon for it.

Side question - is there any way to collapse sections within a custom form?

Our forms can get very long and when we need to access a section that is toward the bottom of the form we need to scroll quite a bit. It would be great if we can collapse the sections to only see the section headers and only expand the section we are looking for.

There isn't, but…

You can set display logic to display sections and/or fields that aren't needed based on what you choose in a control field. It's bit of a hack but if you create a radio button field called "Show Widget Section" and then only display the Widget section when that "yes" button is clicked, you can achieve the same thing.