It's not a question of singlepage/multipage, it's a question of source code organisation
To exagerate a little: it is like asking if you should have only one source file, since your result is only one executable.
How you present the page to the customer (1 page with js/4 pages with links) is a presentational issue, that should not interfere with how you organise your code.
How you keep your source files should determined by how easy it is for the coders to read, extend, debug them.
And how you meet these needs is determined by the actual tasks at hand, and not nesessarly by whether you present them to the user in a single page.
So, without talking about the projects details, i think, it's not easy to answer your question.
As a general guide how, imho, HTML-Templates should be structured, i would suggest the following:
The general page layout should be structured to provide some kind of inheritance, so that i easily can create new pages with the same header, columns, footer, etc, where only placeholders need to be filled.
each "widget" the page uses should be a functional unit, not depending on it's environment. for example, if you have tags, you should only change a single place in your source if you want all your tags to be dispayed as lowercase
Depending on your Technology Stack, these constrains may already imply a certain file structure: in Jinja2 (python templating engine), the general page layout inheritance needs seperate files, in Rails, the rendering of the widgets would be realised via "partials", which would be separate files, too.
Generally, i prefer small files, but that's more a preference. Before overengineering, just start simple (i.e., one file), and dont hesitate to split, as soon as it starts getting messy.