Search St. John's County Homes With Guest Suite, $400,000 - $500,000

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• $900,000 - $1,000,000
• Over $1,000,000

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$450,000

14 Coquina Avenue, St. Augustine

2 Beds 1 Bath 1,056 SqFt Residential MLS® # 2162121

$479,000

180 Spruce Hill Point, St. Johns

3 Beds 3 Baths 2,091 SqFt Residential MLS® # 2162083

$485,000

105 Calley Court, St. Johns

4 Beds 3 Baths 2,294 SqFt Residential MLS® # 2162079

$439,990

↓ $18,000

63 Walloon Cove, St. Augustine

4 Beds 3 Baths 1,875 SqFt Residential MLS® # 2161948

Under Contract

$474,900

105 Bloomfield Way, St. Augustine

4 Beds 4 Baths 2,270 SqFt Residential MLS® # 2161778

Open House

$469,990

782 Farmfield Drive, St. Augustine

4 Beds 3 Baths 2,190 SqFt Residential

Open House

Fri, Sep 11th, 2026 @ 1pm - 5pm

MLS® # 2161691

Open House

$479,990

643 Farmfield Drive, St. Augustine

3 Beds 3 Baths 2,316 SqFt Residential

Open House

Fri, Sep 11th, 2026 @ 1pm - 5pm

MLS® # 2161681

$439,000

542 Silver Landing Drive, St. Augustine

4 Beds 3 Baths 2,098 SqFt Residential MLS® # 2161680

$479,900

136 Southern Grove Drive, St. Augustine

4 Beds 2 Baths 1,722 SqFt Residential MLS® # 2161613

Pending

$462,990

85 Stiffs Mill Lane, St. Augustine

3 Beds 2 Baths 1,897 SqFt Residential MLS® # 2161557

$424,990

554 Barbosa Trail, St. Augustine

4 Beds 3 Baths 2,201 SqFt Residential MLS® # 2161533

$495,000

129 Oyster Shell Terrace, Ponte Vedra

2 Beds 2 Baths 1,534 SqFt Residential MLS® # 2161443

$465,100

↑ $100

5149 Avenue D, St. Augustine

5 Beds 4 Baths 2,869 SqFt Residential MLS® # 2161428

Open House

$499,990

228 Donovan Drive, St. Augustine

4 Beds 3 Baths 1,968 SqFt Residential

Open House

Fri, Sep 11th, 2026 @ 1pm - 5pm

MLS® # 2161334

$459,900

114 Bluejack Lane, St. Augustine

4 Beds 2 Baths 2,008 SqFt Residential MLS® # 2161324

Under Contract

$425,000

200 Nottingham Drive W, St. Johns

4 Beds 3 Baths 1,987 SqFt Residential MLS® # 2161272

$500,000

502 Knotted Birch Avenue, St. Augustine

2 Beds 2 Baths 1,809 SqFt Residential MLS® # 2161212

$495,000

216 Amberwood Drive, St. Augustine

2 Beds 2 Baths 1,779 SqFt Residential MLS® # 2161210

$449,000

127 Sweet Mango Trail, St. Augustine

5 Beds 3 Baths 2,512 SqFt Residential MLS® # 2138029

$425,000

4460 Cedar Ford Boulevard, Hastings

3 Beds 2 Baths 1,695 SqFt Residential MLS® # 2161167

Under Contract

$449,900

4532 Comanche Trail Boulevard, St. Johns

3 Beds 2 Baths 1,753 SqFt Residential MLS® # 2161161

Under Contract

$485,000

193 Miraloma Lane, Ponte Vedra Beach

4 Beds 2 Baths 1,595 SqFt Residential MLS® # 2161097

$450,000

148 Martin Luther King Avenue, St. Augustine

3 Beds 2 Baths 1,048 SqFt Residential MLS® # 2161062

$485,000

↓ $10,000

223 Meadow Crossing Drive, St. Augustine

4 Beds 2 Baths 2,270 SqFt Residential MLS® # 2161052

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