diff --git a/docs/docsite/_static/ansible.css b/docs/docsite/_static/ansible.css
index 3fea13034ad..336d35efd2c 100644
--- a/docs/docsite/_static/ansible.css
+++ b/docs/docsite/_static/ansible.css
@@ -4,13 +4,63 @@
 /* override table width restrictions */
 @media screen and (min-width: 767px) {
 
+  /* If we ever publish to read the docs, we need to use !important for these
+   * two styles as read the docs itself loads their theme in a way that we
+   * can't otherwise override it.
+   */
    .wy-table-responsive table td {
-      /* !important prevents the common CSS stylesheets from overriding
-         this as on RTD they are loaded after this stylesheet */
-      white-space: normal !important;
+      white-space: normal;
    }
 
    .wy-table-responsive {
-      overflow: visible !important;
+      overflow: visible;
    }
 }
+
+/*
+ * We use the class documentation-table for attribute tables where the first
+ * column is the name of an attribute and the second column is the description.
+ */
+
+/* These tables look like this:
+ * 
+ *  Attribute Name     Description
+ *  --------------     -----------
+ *  **NAME**           This is a multi-line description
+ *  str/required       that can span multiple lines
+ *
+ *                     With multiple paragraphs
+ *  --------------     -----------
+ *
+ * **NAME** is given the class .value-name
+ * str is given the class .value-type
+ * / is given the class .value-separator
+ * required is given the class .value-required
+ */
+
+table.documentation-table td:first-child {
+    white-space: nowrap;
+    vertical-align: top;
+}
+
+table.documentation-table .value-name {
+    font-weight: bold;
+    display: inline;
+}
+
+table.documentation-table .value-type {
+    font-size: x-small;
+    color: purple;
+    display: inline;
+}
+
+table.documentation-table .value-separator {
+    font-size: x-small;
+    display: inline;
+}
+
+table.documentation-table .value-required {
+    font-size: x-small;
+    color: red;
+    display: inline;
+}
diff --git a/docs/templates/collections_galaxy_meta.rst.j2 b/docs/templates/collections_galaxy_meta.rst.j2
index 87c530e0760..cb3568b32ad 100644
--- a/docs/templates/collections_galaxy_meta.rst.j2
+++ b/docs/templates/collections_galaxy_meta.rst.j2
@@ -16,38 +16,44 @@ Structure
 
 The ``galaxy.yml`` file must contain the following keys in valid YAML:
 
-.. raw:: html
-
-    <table  border=0 cellpadding=0 class="documentation-table">
-        {# Header of the documentation -#}
-        <tr>
-            <th>Key</th>
-            <th width="100%">Comments</th>
-        </tr>
-        {% for entry in options %}
-            <tr>
-                {# key name with required or type label #}
-                <td>
-                    <b>@{ entry.key }@</b>
-                    <div style="font-size: small">
-                        <span style="color: purple">@{ entry.type | documented_type }@</span>
-                        {% if entry.get('required', False) %} / <span style="color: red">required</span>{% endif %}
-                    </div>
-                </td>
-                {# Comments #}
-                <td>
-                    {% if entry.description is string %}
-                        <div>@{ entry.description | replace('\n', '\n    ') | html_ify }@</div>
-                    {% else %}
-                        {% for desc in entry.description %}
-                            <div>@{ desc | replace('\n', '\n    ') | html_ify }@</div>
-                        {% endfor %}
-                    {% endif %}
-                </td>
-            </tr>
-        {% endfor %}
-    </table>
-    <br/>
+
+.. rst-class:: documentation-table
+
+.. list-table::
+    :header-rows: 1
+    :widths: auto
+
+    * - Key
+      - Comment
+
+{%- for entry in options %}
+
+
+    * - .. rst-class:: value-name
+
+        @{ entry.key }@ |br|
+
+        .. rst-class:: value-type
+
+        @{ entry.type | documented_type }@ |_|
+
+        {% if entry.get('required', False) -%}
+        .. rst-class:: value-separator
+
+        / |_|
+
+        .. rst-class:: value-required
+
+        required
+        {%- endif %}
+
+
+      - {% for desc in entry.description -%}
+        @{ desc | trim | rst_ify }@
+
+        {% endfor -%}
+{%- endfor %}
+
 
 Examples
 ========
diff --git a/docs/templates/plugin.rst.j2 b/docs/templates/plugin.rst.j2
index 65acbb2e220..2edbad34d0d 100644
--- a/docs/templates/plugin.rst.j2
+++ b/docs/templates/plugin.rst.j2
@@ -50,13 +50,9 @@ Synopsis
 --------
 {% if description -%}
 
-{%   if description is string -%}
-- @{ description | rst_ify }@
-{%   else %}
-{%     for desc in description %}
+{%   for desc in description %}
 - @{ desc | rst_ify }@
-{%     endfor %}
-{%   endif %}
+{%   endfor %}
 
 {% endif %}
 
@@ -183,13 +179,9 @@ Parameters
                 {% endif %}
                 {# description #}
                 <td>
-                    {% if value.description is string %}
-                        <div>@{ value.description | replace('\n', '\n    ') | html_ify }@</div>
-                    {% else %}
-                        {% for desc in value.description %}
-                            <div>@{ desc | replace('\n', '\n    ') | html_ify }@</div>
-                        {% endfor %}
-                    {% endif %}
+                    {% for desc in value.description %}
+                        <div>@{ desc | replace('\n', '\n    ') | html_ify }@</div>
+                    {% endfor %}
                     {% if 'aliases' in value and value.aliases %}
                         <div style="font-size: small; color: darkgreen"><br/>aliases: @{ value.aliases|join(', ') }@</div>
                     {% endif %}
diff --git a/hacking/build_library/build_ansible/command_plugins/collection_meta.py b/hacking/build_library/build_ansible/command_plugins/collection_meta.py
index b28797473f2..7b7112e8f9a 100644
--- a/hacking/build_library/build_ansible/command_plugins/collection_meta.py
+++ b/hacking/build_library/build_ansible/command_plugins/collection_meta.py
@@ -12,18 +12,26 @@ import pathlib
 
 import yaml
 from jinja2 import Environment, FileSystemLoader
+from ansible.module_utils.six import string_types
 from ansible.module_utils._text import to_bytes
 
 # Pylint doesn't understand Python3 namespace modules.
 from ..change_detection import update_file_if_different  # pylint: disable=relative-beyond-top-level
 from ..commands import Command  # pylint: disable=relative-beyond-top-level
-from ..jinja2.filters import documented_type, html_ify  # pylint: disable=relative-beyond-top-level
+from ..jinja2.filters import documented_type, rst_ify  # pylint: disable=relative-beyond-top-level
 
 
 DEFAULT_TEMPLATE_FILE = 'collections_galaxy_meta.rst.j2'
 DEFAULT_TEMPLATE_DIR = pathlib.Path(__file__).parents[4] / 'docs/templates'
 
 
+def normalize_options(options):
+    """Normalize the options to make for easy templating"""
+    for opt in options:
+        if isinstance(opt['description'], string_types):
+            opt['description'] = [opt['description']]
+
+
 class DocumentCollectionMeta(Command):
     name = 'collection-meta'
 
@@ -51,12 +59,14 @@ class DocumentCollectionMeta(Command):
         with open(args.collection_defs) as f:
             options = yaml.safe_load(f)
 
+        normalize_options(options)
+
         env = Environment(loader=FileSystemLoader(template_dir),
                           variable_start_string="@{",
                           variable_end_string="}@",
                           trim_blocks=True)
         env.filters['documented_type'] = documented_type
-        env.filters['html_ify'] = html_ify
+        env.filters['rst_ify'] = rst_ify
 
         template = env.get_template(template_file)
         output_name = os.path.join(output_dir, template_file.replace('.j2', ''))
diff --git a/hacking/build_library/build_ansible/command_plugins/plugin_formatter.py b/hacking/build_library/build_ansible/command_plugins/plugin_formatter.py
index 7407c97f997..1d2ed459f8a 100644
--- a/hacking/build_library/build_ansible/command_plugins/plugin_formatter.py
+++ b/hacking/build_library/build_ansible/command_plugins/plugin_formatter.py
@@ -386,8 +386,17 @@ def process_plugins(module_map, templates, outputname, output_dir, ansible_versi
             if field in doc and doc[field] in (None, ''):
                 print("%s: WARNING: MODULE field '%s' DOCUMENTATION is null/empty value=%s" % (fname, field, doc[field]))
 
+        if 'description' in doc:
+            if isinstance(doc['description'], string_types):
+                doc['description'] = [doc['description']]
+            elif not isinstance(doc['description'], (list, tuple)):
+                raise AnsibleError("Description must be a string or list of strings.  Got %s"
+                                   % type(doc['description']))
+        else:
+            doc['description'] = []
+
         if 'version_added' not in doc:
-            display.error("*** ERROR: missing version_added in: %s ***\n" % module)
+            raise AnsibleError("*** ERROR: missing version_added in: %s ***\n" % module)
 
         #
         # The present template gets everything from doc so we spend most of this
@@ -416,6 +425,14 @@ def process_plugins(module_map, templates, outputname, output_dir, ansible_versi
                 if 'description' not in doc['options'][k]:
                     raise AnsibleError("Missing required description for parameter '%s' in '%s' " % (k, module))
 
+                # Make sure description is a list of lines for later formatting
+                if isinstance(doc['options'][k]['description'], string_types):
+                    doc['options'][k]['description'] = [doc['options'][k]['description']]
+                elif not isinstance(doc['options'][k]['description'], (list, tuple)):
+                    raise AnsibleError("Invalid type for options['%s']['description']."
+                                       " Must be string or list of strings.  Got %s" %
+                                       (k, type(doc['options'][k]['description'])))
+
                 # Error out if required isn't a boolean (people have been putting
                 # information on when something is required in here.  Those need
                 # to go in the description instead).
@@ -427,10 +444,6 @@ def process_plugins(module_map, templates, outputname, output_dir, ansible_versi
                 if 'version_added' in doc['options'][k] and too_old(doc['options'][k]['version_added']):
                     del doc['options'][k]['version_added']
 
-                # Make sure description is a list of lines for later formatting
-                if not isinstance(doc['options'][k]['description'], list):
-                    doc['options'][k]['description'] = [doc['options'][k]['description']]
-
                 option_names.append(k)
 
         option_names.sort()
diff --git a/hacking/build_library/build_ansible/jinja2/filters.py b/hacking/build_library/build_ansible/jinja2/filters.py
index 735d07b7ba7..21436eda907 100644
--- a/hacking/build_library/build_ansible/jinja2/filters.py
+++ b/hacking/build_library/build_ansible/jinja2/filters.py
@@ -27,7 +27,7 @@ _ITALIC = re.compile(r"I\(([^)]+)\)")
 _BOLD = re.compile(r"B\(([^)]+)\)")
 _MODULE = re.compile(r"M\(([^)]+)\)")
 _URL = re.compile(r"U\(([^)]+)\)")
-_LINK = re.compile(r"L\(([^)]+),([^)]+)\)")
+_LINK = re.compile(r"L\(([^)]+), *([^)]+)\)")
 _CONST = re.compile(r"C\(([^)]+)\)")
 _RULER = re.compile(r"HORIZONTALLINE")