The existing CN and CP lines between Cobourg and Port Hope are a couple km south of the 401, almost right on the lakeshore and there aren't any interchanges between the two towns. The existing VIA station in Cobourg probably makes more sense - it's on a major arterial that meets the 401, but still just a few blocks from downtown.
I would probably agree with keeping stations in the towns and simply designating either Port Hope or Cobourg as an HSR station. I know that there are cases where European HSR lines have stations in fields between two cities but the practice has also been criticized. It would be worth looking at more and seeing just how effective that model is.
Actually I had never really considered Cobourg or Port Hope as being places to put an HSR station. The only reason I mentioned an upgaded line terminating at Cobourg was because it made sense in terms of building an upgraded inner city infrastructure. Essentially I thought that the first dedicated passenger rail section would run from Cobourg to Union Station and though built to a minimum standard of 160 km/h most places along the line would be served by either VIA local or GO services. Once primary HSR lines where built between cities then I would have had an HSR bypass built from just east of Cobourg to roughly Oshawa. But an HSR station in the Cobourg/Port Hope area does seem to make sense (especially as those two cities grow).
How far apart are HSR stations close to major cities in Europe? If the dominant model has quite a few stations to serve commuters then the line going through Peterborough wouldn't make any sense. There's really nothing between Peterborough and Ottawa but a lakeshore line could have stops in Oshawa, Cobourg/Port Hope, Belleville, Kingston, and Ottawa.
It depends quite a bit, but, a general rule would be that once a train leaves the central station it will possibley serve a suburban node within the city (or an airport) and then after that the distance of HSR stations is roughly 100km between each. But each line is likely to be different.
One easy way to deal with the issue is to simply rate stations/cities for their potential HSR market. So major points like Union, Pearson, Kingston, Ottawa, etc, would have full HSR stations and it would be assumed that most HSR trains would stop at these points. But there could be other stations, such as Oshawa, Port Hope/Cobourg, perhaps some suburban stations where HSR might be useful some of the time, but not all the time. In those cases you just build the stations with platforms that can accomodate HSR trains, but not necessarily the other service options of high order HSR stations. This way HSR can make use of some of the smaller stations when it makes sense from a service point of view, and ignoring them when it doesn't.
And with a proper passenger rail and HSR network it becomes less an issue of where to put stations and simply an issue of creating schedules that meet customer demand and provide fast service. It would be very likely that there would be some early morning, and late evening, commuter trains between Toronto - Montreal or Toronto - Ottawa that would go from central station to central station with no stops in between. There could be other trains that would make stops at more suburban nodes such as Guildwood, Oshawa, Dorval, etc, thus capturing a different market.
That is really why the Lakeshore line makes far more sense. If it is designed properly to allow for flexibilty in scheduling and train configurations, you can serve not just downtown to downtown markets between the major cities, but points in between which would greatly enhance the value of the service.
Edit: Another possibility to consider would be to connect Peterborough to the rail network via a line that would run from Port Hope to Peterborugh roughly along the Highway 28 routing. It might not be the fastest route for commuters (though would still not be bad on a proper network), but, if it was shown that a lot of growth would come from people from Peterborough also wanting to connect to other VIA services (taking a train to Montreal or using the train to get to Pearson) then it could be a way to serve both commuters and long distance travellers. In that case an HSR station in Port Hope could make sense since it would already serve as a transfer point for a group of passengers.