diff --git a/lib/matplotlib/sphinxext/plot_directive.py b/lib/matplotlib/sphinxext/plot_directive.py
index d8f3048ad556..28aeeb394478 100644
--- a/lib/matplotlib/sphinxext/plot_directive.py
+++ b/lib/matplotlib/sphinxext/plot_directive.py
@@ -71,6 +71,11 @@
         If specified, the code block will be run, but no figures will be
         inserted.  This is usually useful with the ``:context:`` option.
 
+    caption : str
+        If specified, the option's argument will be used as a caption for the
+        figure. This overwrites the caption given in the content, when the plot
+        is generated from a file.
+
 Additionally, this directive supports all of the options of the `image`
 directive, except for *target* (since plot will add its own target).  These
 include *alt*, *height*, *width*, *scale*, *align* and *class*.
@@ -240,12 +245,16 @@ class PlotDirective(Directive):
         'context': _option_context,
         'nofigs': directives.flag,
         'encoding': directives.encoding,
+        'caption': directives.unchanged,
         }
 
     def run(self):
         """Run the plot directive."""
-        return run(self.arguments, self.content, self.options,
-                   self.state_machine, self.state, self.lineno)
+        try:
+            return run(self.arguments, self.content, self.options,
+                       self.state_machine, self.state, self.lineno)
+        except Exception as e:
+            raise self.error(str(e))
 
 
 def setup(app):
@@ -636,6 +645,16 @@ def run(arguments, content, options, state_machine, state, lineno):
         # If there is content, it will be passed as a caption.
         caption = '\n'.join(content)
 
+        # Enforce unambiguous use of captions.
+        if "caption" in options:
+            if caption:
+                raise ValueError(
+                    'Caption specified in both content and options.'
+                    ' Please remove ambiguity.'
+                )
+            # Use caption option
+            caption = options["caption"]
+
         # If the optional function name is provided, use it
         if len(arguments) == 2:
             function_name = arguments[1]
@@ -652,7 +671,7 @@ def run(arguments, content, options, state_machine, state, lineno):
         base, ext = os.path.splitext(os.path.basename(source_file_name))
         output_base = '%s-%d.py' % (base, counter)
         function_name = None
-        caption = ''
+        caption = options.get('caption', '')
 
     base, source_ext = os.path.splitext(output_base)
     if source_ext in ('.py', '.rst', '.txt'):
diff --git a/lib/matplotlib/tests/test_sphinxext.py b/lib/matplotlib/tests/test_sphinxext.py
index fd9e9344e5ac..3ce8d2951d07 100644
--- a/lib/matplotlib/tests/test_sphinxext.py
+++ b/lib/matplotlib/tests/test_sphinxext.py
@@ -21,6 +21,7 @@ def test_tinypages(tmpdir):
            str(Path(__file__).parent / 'tinypages'), str(html_dir)]
     proc = Popen(cmd, stdout=PIPE, stderr=PIPE, universal_newlines=True)
     out, err = proc.communicate()
+
     assert proc.returncode == 0, \
         "sphinx build failed with stdout:\n{}\nstderr:\n{}\n".format(out, err)
     if err:
@@ -52,3 +53,7 @@ def plot_file(num):
     assert filecmp.cmp(range_6, html_dir / 'range6.png')
     # check if figure caption made it into html file
     assert b'This is the caption for plot 15.' in html_contents
+    # check if figure caption using :caption: made it into html file
+    assert b'Plot 17 uses the caption option.' in html_contents
+    # check if figure caption made it into html file
+    assert b'This is the caption for plot 18.' in html_contents
diff --git a/lib/matplotlib/tests/tinypages/some_plots.rst b/lib/matplotlib/tests/tinypages/some_plots.rst
index 615908b0107f..5a71abc9e761 100644
--- a/lib/matplotlib/tests/tinypages/some_plots.rst
+++ b/lib/matplotlib/tests/tinypages/some_plots.rst
@@ -127,3 +127,17 @@ Plot 16 uses a specific function in a file with plot commands:
 .. plot:: range6.py range6
 
 
+Plot 17 gets a caption specified by the :caption: option:
+
+.. plot::
+   :caption: Plot 17 uses the caption option.
+
+   plt.figure()
+   plt.plot(range(6))
+
+
+Plot 18 uses an external file with the plot commands and a caption
+using the :caption: option:
+
+.. plot:: range4.py
+   :caption: This is the caption for plot 18.