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Thanks to simplexio and Vince for their useful comments leading to this answer: Shapefile is not a multiuser file format and multiuser access leads to a range of problems beginning with slow access due to file locking problems up to massive data loss. Its recommended to set up a database-server (eg PostGIS) The data is then streamed to Q-GIS for multiuser ...
Literally the stupidest of problems. Forgot to include the layer in the url. As the documentation clearly points out, the URL format works like this: http://localhost:<port>/<layer-name>/<z>/<x>/<y>/<route-name> With that small change, I now have it working on my Mapbox.js map without any problems.
I thought I would add a late answer here to expand upon my comments from last year. After re-reading this, I thought of a few good examples of sites that I know of that would be beneficial as examples to anyone viewing this question. The City of Hudson, Ohio has an interesting GIS website. They incorporate city work orders, city layers, community info, ...
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