Upgraded ESRI .NET ADF application (9.3 to 10.1) intermittently missing service issue

Question

I also asked this question on the ESRI forum but I'm not sure if anyone will see it through the tumbleweeds over there.

I had an application based on the .NET Web ADF originally built in 9.3. The server is being upgraded to 10.1 so the application needs to move with it (re-architecting is not an option).

The automated upgrade utility for moving ADF applications to 10.1 was not the smoothest process and I have since fixed a couple of very obvious bugs in the ESRI JavaScript. However there is one problem I can't figure out:

Intermittently, after a full page reload, the map fails to render. The application calls ESRI.ArcGIS.ADF.Web.UI.WebControls.MapHandler.ashx requesting a URL for the new map image. Sometimes that handler returns

{"code":400,"type":"error","errorMessage":"Resource <service name> not found"}

The application then requests an image from ESRI.ArcGIS.ADF.Web.MimeImage.ashx passing an ImgID parameter that seems to be randomly made-up - I can't see it in any previous requests and it obviously isn't provided by MapHandler.ashx. The server then responds with a 404. If I reload the application again the same requests are sent with exactly the same parameters (in the example I saw the post-reload request even passed the same 't' parameter which I assume should represent time) and a successful response is returned.

Can anyone tell me why my service is intermittently reported as unavailable? ArcGIS Server is not logging any errors or warnings. Based on this and how quickly the request is re-issued and successfully answered I don't think the service is actually having trouble. Comparing a working and a failing request in Fiddler gives me no clues as the same headers and cookies seem to be sent.

EDIT The only reason I can imagine is if the server control 'MapResourceManager' or something associated with it isn't fully initialised by the time the first request is sent, but as such timing issues are the responsibility of the framework I would be surprised if this was the problem. However I've seen widespread use of setTimeout in the ADF's JavaScript and I'm really hoping this issue isn't the result of some flawed assumption about timing.