diff --git a/elements/hosts/os-apply-config/var/run/hosts.d/tail b/elements/hosts/os-apply-config/var/run/hosts.d/tail
deleted file mode 100644
index 9db1e07eb..000000000
--- a/elements/hosts/os-apply-config/var/run/hosts.d/tail
+++ /dev/null
@@ -1 +0,0 @@
-{{hosts}}
diff --git a/elements/hosts/os-refresh-config/configure.d/51-hosts b/elements/hosts/os-refresh-config/configure.d/51-hosts
index 49bb4b22d..de6cb9062 100755
--- a/elements/hosts/os-refresh-config/configure.d/51-hosts
+++ b/elements/hosts/os-refresh-config/configure.d/51-hosts
@@ -1,24 +1,49 @@
 #!/bin/bash
 
-set -eu
+set -eux
 set -o pipefail
 
-# 51 - right after oac as hosts is needed for $justabouteverything.
+write_entries() {
+    local file="$1"
+    local entries="$2"
 
-if [ ! -e /etc/hosts -o ! -e /var/run/hosts.d/tail ]; then
-    exit 0
-fi
+    # Don't do anything if the file isn't there
+    if [ ! -f "$file" ]; then
+        return
+    fi
 
-if fgrep -f /var/run/hosts.d/tail /etc/hosts; then
-    exit 0
-fi
-cp /etc/hosts /var/run/hosts.d/new-hosts
-echo >> /var/run/hosts.d/new-hosts
-cat /var/run/hosts.d/tail >> /var/run/hosts.d/new-hosts
-echo >> /var/run/hosts.d/new-hosts
-mv /var/run/hosts.d/new-hosts /etc/hosts
+    if grep -q "^# HEAT_HOSTS_START" "$file"; then
+        temp=$(mktemp)
+        awk -v v="$entries" '/^# HEAT_HOSTS_START/ {
+            print $0
+            print v
+            f=1
+            }f &&!/^# HEAT_HOSTS_END$/{next}/^# HEAT_HOSTS_END$/{f=0}!f' "$file" > "$temp"
+            echo "INFO: Updating hosts file $file, check below for changes"
+            diff "$file" "$temp"
+            cat "$temp" > "$file"
+    else
+        echo -ne "\n# HEAT_HOSTS_START - Do not edit manually within this section!\n" >> "$file"
+        echo "$entries" >> "$file"
+        echo -ne "# HEAT_HOSTS_END\n\n" >> "$file"
+    fi
 
-# /etc/hosts may have the wrong SELinux file contexts.
-if [ -x /usr/sbin/semanage ]; then
-    restorecon -v /etc/hosts
+}
+
+ENTRIES=$(os-apply-config --key hosts --type raw --key-default '')
+if [ ! -z "$ENTRIES" ]; then
+    # cloud-init files are /etc/cloud/templates/hosts.OSNAME.tmpl
+    DIST=$(lsb_release -is | tr -s [A-Z] [a-z])
+    case $DIST in
+        fedora)
+            name="redhat"
+            ;;
+        *)
+            name="$DIST"
+            ;;
+    esac
+    write_entries "/etc/cloud/templates/hosts.${name}.tmpl" "$ENTRIES"
+    write_entries "/etc/hosts" "$ENTRIES"
+else
+    echo "No hosts in Heat, nothing written."
 fi