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Since I am not employed now, nor am I allowed to hold a full-time position, I will not be able to show sufficient funds from my personal account. In this case, do my boyfriend and I (we will be married by the time I apply) each need to show our funds separately, in addition to his mother's supporting funds? Is it better for he and I to pool our funds into a joint account?
In general, it is usually the UK sponsor's (your husband's) salary that is used to show the maintenance funds since he is the UK citizen sponsoring the visa (i.e. he is more likely than the US citizen to have a job, home and life already set up in the UK), however, your joint finances together are considered for the visa. You don't need to have a joint account, you would just send your individual bank statements for the last 3-6 months.
However, if your mother will be a third party sponsor (assuming a non-UK family member is allowed to provide third party support - usually it's provided by family members residing in the UK), then it will be her original bank statements and payslips that will be considered for the visa rather than yours.
His mother is purchasing a flat for us to live in and she will be paying the mortgage. While he will be making informal contributions to his mother of around £400/month there will be no contractual obligation for him to pay in any way for the accommodation (the flat is basically a gift). How would we demonstrate/document this for the UKBA?
His mother will need to provide the evidence of her home-ownership, mortgage statements and the land registry document for the property. She will also need to write a letter of support, explaining that she is giving you permission to live in the property and that you will be contributing £400/month towards the costs.
Also, would this (beneficial) situation affect the assessment of the adequacy of our own, relatively meagre, maintenance funds?
Well, the only affect it will have is that you will only need to take into account the money you will be paying his mother per month rather than the usual rent and council tax.
Assuming you apply before the rules change (expected to come into effect in June), you will just need to show that you have at least £111 left over each week after paying any rent/council tax to his mother.
However, from June, the sponsor (your husband) may be required to earn a minimum salary of somewhere between £18,000 and £25,000 (£25,600 is the figure being discussed at the moment) and we don't know if third party support will still be allowed or not from June yet.