How do I prevent 404's from hurting my site?
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I manage a real estate broker's site on which the individual MLS listing pages continually create 404 pages as properties are sold. So, on a site with 2200 pages indexed, roughly half are 404s at any given time. What can I do to mitigate any potential harm from this?
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You could setup 301 redirects from the sold property URLs to another relevant page, like other properties available in the same neighborhood/town/city. Or possibly even to search result page that contains very similar properties in regards to square footage, bedrooms, baths, etc.
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I should have mentioned that I don't have that option. The pages are dynamically added to the site via a plugin which pulls MLS data from the local real estate listing board. (The plugin is dsIDXpress by Diverse Solutions.)
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I'd create a custom 404 page which runs a similar search, whilst you say you can't avoid the 404 what you can do is make a 404 which is useful to both the user and Google
Also make sure that your site no longer lings to old content.Run Screaming Frog to check those response codes

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Property sites use a range of techniques to handle this - I have seen 404s, 410 Gone responses, 302 redirects and 200 OK responses showing a largely blank page (definitely not recommended) whilst browsing a little this morning.
Others leave the listing live but show that it's no longer on the market, e.g. http://www.rightmove.co.uk/property-to-rent/property-29033160.html
It doesn't sound like you can use this last option, although it would allow you to recycle URLs for properties like rentals that often come back on the market.
If you must go with a 404, try to make it useful as Dave says. Can you customise the 404 page, perhaps pulling in information dynamically based upon the listing that was deleted?
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I support Jane's advice here to make a custom 404 that is as beneficial as possible for the user.
I would only worry about 301 redirecting old property pages to their city/neighborhood subcategory if the page shows up in Google Webmaster Tools 404 section and shows an external link pointing at it that is worth saving. A process you could do about once per month or quarter.