Just want to revive this question as a few users who I help support are also encountering it…
Peter Hannah did you ever determine what the cause was, and did this issue continue to happen?
For us, it appears to occur when loading a Feature Layer from an ArcGIS Server REST API containing many features (200,000+) in a webmap. When opening the map in Chrome, the layer usually loads fine the first time. Then on subsequent loads, the error you described in your original message occurs. Clearing the cache in Chrome appears to work every time to then get the map to properly load the layer, but the error then soon re-occurs again after a few subsequent map loads.
Also, I am wondering if it is related to the computer hardware people are using. Personally I never experienced the problem using 64-bit Firefox on 64-bit macOS, with 8GB of memory and a Core i7 processor. However another user I know is running 32-bit Windows 7, uncertain how much memory – but it is not as high-end of a machine, and the problem frequently occurs in Chrome (unsure about Firefox).
Curious if others have any thoughts, too…