This can't be good, maybe from when I blew out the fuel lines with compressed air? Fine rusty dusty.

Am I correct in assuming this rust is originating post fuel filter?

Yes. Iron oxide can only come post filter. Unless the filter has holes in it.

White aluminium oxide is common to clog up float bowls. Also the result of water in the fuel. It settles in the carby and white crap builds up in the bowl.

Just clean out the carby and get over it

Is it possible that the rust built up inside the mechanical fuel pump as a result of being left empty unsealed and open to the weather? Sounds like a possible cause to me. The rust in the lines is a hugely small possibility.

Keeping fuel in the rail/system will prevent it from getting worse.