diff --git a/message/classes/helper.php b/message/classes/helper.php
index a7b7a84286c..8c74eb4110b 100644
--- a/message/classes/helper.php
+++ b/message/classes/helper.php
@@ -151,6 +151,7 @@ class helper {
         // Check if the user is online.
         $data->isonline = \core_message\helper::is_online($userfields->lastaccess);
         $data->isread = isset($contact->isread) ? $contact->isread : 0;
+        $data->unreadcount = isset($contact->unreadcount) ? $contact->unreadcount : null;
 
         return new \core_message\output\messagearea\contact($data);
     }
diff --git a/message/classes/output/messagearea/contact.php b/message/classes/output/messagearea/contact.php
index 5a2f016aef4..a6a64ef2949 100644
--- a/message/classes/output/messagearea/contact.php
+++ b/message/classes/output/messagearea/contact.php
@@ -76,6 +76,7 @@ class contact implements templatable, renderable {
         }
         $contact->isonline = $this->contact->isonline;
         $contact->isread = $this->contact->isread;
+        $contact->unreadcount = $this->contact->unreadcount;
 
         return $contact;
     }
diff --git a/message/externallib.php b/message/externallib.php
index dea9798f4ce..17053a86ec5 100644
--- a/message/externallib.php
+++ b/message/externallib.php
@@ -752,6 +752,7 @@ class core_message_external extends external_api {
                             'lastmessage' => new external_value(PARAM_RAW, 'The user\'s last message, null if none.'),
                             'isonline' => new external_value(PARAM_BOOL, 'The user\'s online status'),
                             'isread' => new external_value(PARAM_BOOL, 'If the user has read the message'),
+                            'unreadcount' => new external_value(PARAM_INT, 'The number of unread messages in this conversation'),
                         )
                     )
                 )
diff --git a/message/lib.php b/message/lib.php
index 48b4a10d992..c6e4b927910 100644
--- a/message/lib.php
+++ b/message/lib.php
@@ -411,6 +411,12 @@ function message_get_recent_conversations($user, $limitfrom=0, $limitto=100) {
     $sql = str_replace('1 as readtable', '0 as readtable', $sql);
     $unread = $DB->get_records_sql($sql, $params, $limitfrom, $limitto);
 
+    $unreadcountssql = 'SELECT useridfrom, count(*) as count
+                        FROM {message}
+                        WHERE useridto = :userid
+                        GROUP BY useridfrom';
+    $unreadcounts = $DB->get_records_sql($unreadcountssql, array('userid' => $user->id));
+
     // Union the 2 result sets together looking for the message with the most
     // recent timecreated for each other user.
     // $conversation->id (the array key) is the other user's ID.
@@ -419,8 +425,9 @@ function message_get_recent_conversations($user, $limitfrom=0, $limitto=100) {
     foreach ($conversation_arrays as $conversation_array) {
         foreach ($conversation_array as $conversation) {
             // Only consider it unread if $user has unread messages.
-            if (!$conversation->readtable && $conversation->useridto == $user->id) {
+            if (isset($unreadcounts[$conversation->useridfrom])) {
                 $conversation->isread = 0;
+                $conversation->unreadcount = $unreadcounts[$conversation->useridfrom]->count;
             } else {
                 $conversation->isread = 1;
             }
@@ -429,6 +436,13 @@ function message_get_recent_conversations($user, $limitfrom=0, $limitto=100) {
                 $conversations[$conversation->id] = $conversation;
             } else {
                 $current = $conversations[$conversation->id];
+                // We need to maintain the isread and unreadcount values from existing
+                // parts of the conversation if we're replacing it.
+                $conversation->isread = ($conversation->isread && $current->isread);
+                if (isset($current->unreadcount) && !isset($conversation->unreadcount)) {
+                    $conversation->unreadcount = $current->unreadcount;
+                }
+
                 if ($current->timecreated < $conversation->timecreated) {
                     $conversations[$conversation->id] = $conversation;
                 } else if ($current->timecreated == $conversation->timecreated) {
diff --git a/message/templates/message_content_item.mustache b/message/templates/message_content_item.mustache
index 856515ae1c6..e32faf72801 100644
--- a/message/templates/message_content_item.mustache
+++ b/message/templates/message_content_item.mustache
@@ -50,6 +50,9 @@
             <h3>{{fullname}}</h3>
             <p>{{lastmessage}}</p>
         </div>
+        <div class="unread-count-container">
+            <span data-region="unread-count" class="badge badge-important">{{unreadcount}}</span>
+        </div>
     </div>
     {{#contexturl}}
     </a>
diff --git a/theme/bootstrapbase/less/moodle/popover_region.less b/theme/bootstrapbase/less/moodle/popover_region.less
index bc3822b1d2c..87754fa01e5 100644
--- a/theme/bootstrapbase/less/moodle/popover_region.less
+++ b/theme/bootstrapbase/less/moodle/popover_region.less
@@ -637,6 +637,7 @@
                                 height: 100%;
                                 width: 20%;
                                 display: inline-block;
+                                text-align: center;
 
                                 img {
                                     height: 100%;
@@ -664,9 +665,23 @@
                                     margin: 0;
                                 }
                             }
+
+                            .unread-count-container {
+                                display: none;
+                            }
                         }
                         &.unread {
                             background-color: #f1f1f1;
+
+                            .content-item-body {
+                                width: 65%;
+                            }
+
+                            .unread-count-container {
+                                display: inline-block;
+                                width: 10%;
+                                text-align: center;
+                            }
                         }
                     }
                 }
diff --git a/theme/bootstrapbase/style/moodle.css b/theme/bootstrapbase/style/moodle.css
index f5f6d1d4ed1..e065b7a1740 100644
--- a/theme/bootstrapbase/style/moodle.css
+++ b/theme/bootstrapbase/style/moodle.css
@@ -7848,6 +7848,7 @@ body.path-question-type .mform fieldset.hidden {
   height: 100%;
   width: 20%;
   display: inline-block;
+  text-align: center;
 }
 .popover-region-messages.popover-region .popover-region-container .popover-region-content-container .popover-region-content .content-item-container .content-item .profile-image-container img {
   height: 100%;
@@ -7871,9 +7872,20 @@ body.path-question-type .mform fieldset.hidden {
 .popover-region-messages.popover-region .popover-region-container .popover-region-content-container .popover-region-content .content-item-container .content-item .content-item-body p {
   margin: 0;
 }
+.popover-region-messages.popover-region .popover-region-container .popover-region-content-container .popover-region-content .content-item-container .content-item .unread-count-container {
+  display: none;
+}
 .popover-region-messages.popover-region .popover-region-container .popover-region-content-container .popover-region-content .content-item-container.unread {
   background-color: #f1f1f1;
 }
+.popover-region-messages.popover-region .popover-region-container .popover-region-content-container .popover-region-content .content-item-container.unread .content-item-body {
+  width: 65%;
+}
+.popover-region-messages.popover-region .popover-region-container .popover-region-content-container .popover-region-content .content-item-container.unread .unread-count-container {
+  display: inline-block;
+  width: 10%;
+  text-align: center;
+}
 .popover-region-messages.popover-region .popover-region-container .popover-region-content-container.loading .popover-region-content .messages:empty + .empty-message {
   display: none;
 }