This is pretty common. For resource style sheets, etc. This is usually the result of not using @ Content.Url. I assume that for other problems you can hardcode your links, rather than using @ Url.Action. This is again a common occurrence, I have encountered it several times.
Indeed, basically in the development environment you are not actually interested in virtual directories, however in the production environment this is more of a problem.
I would think that / Account / Login points to the root directory when using IIS IIS, which you want to point to this route through the virtual directory. If the link is created through something like <% = Html.ActionLink%>, then you're fine. But if you have javascript and you call the url, or if your hardcoding your links to MyController / MyList, then it will not find it.
Same thing with css files. If you look at how the Site.css file is accessed when creating a new project, you will see something like this:
<link href = '<% = Url.Content ("~ / Content.Site.css")%>' , etc. etc.
Let me know if that makes sense.
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