diff --git a/tools/linter_lib/custom_check.py b/tools/linter_lib/custom_check.py
index d8a728a735..59ad1401dd 100644
--- a/tools/linter_lib/custom_check.py
+++ b/tools/linter_lib/custom_check.py
@@ -694,7 +694,7 @@ html_rules: List["Rule"] = [
             "templates/corporate/billing.html",
             "templates/corporate/upgrade.html",
             # Miscellaneous violations to be cleaned up
-            "web/templates/user_card_popover_avatar.hbs",
+            "web/templates/popovers/user_card/user_card_popover_avatar.hbs",
             "web/templates/confirm_dialog/confirm_subscription_invites_warning.hbs",
             "templates/zerver/reset_confirm.html",
             "templates/zerver/config_error.html",
diff --git a/web/src/add_stream_options_popover.js b/web/src/add_stream_options_popover.js
index c4c0870e64..377ffa2718 100644
--- a/web/src/add_stream_options_popover.js
+++ b/web/src/add_stream_options_popover.js
@@ -1,6 +1,6 @@
 import $ from "jquery";
 
-import render_left_sidebar_stream_setting_popover from "../templates/left_sidebar_stream_setting_popover.hbs";
+import render_left_sidebar_stream_setting_popover from "../templates/popovers/left_sidebar_stream_setting_popover.hbs";
 
 import * as popover_menus from "./popover_menus";
 import * as settings_data from "./settings_data";
diff --git a/web/src/compose_popovers.js b/web/src/compose_popovers.js
index 751500e1da..78103ea075 100644
--- a/web/src/compose_popovers.js
+++ b/web/src/compose_popovers.js
@@ -1,9 +1,9 @@
 import $ from "jquery";
 import {delegate} from "tippy.js";
 
-import render_compose_control_buttons_popover from "../templates/compose_control_buttons_popover.hbs";
-import render_compose_select_enter_behaviour_popover from "../templates/compose_select_enter_behaviour_popover.hbs";
-import render_mobile_message_buttons_popover from "../templates/mobile_message_buttons_popover.hbs";
+import render_compose_control_buttons_popover from "../templates/popovers/compose_control_buttons/compose_control_buttons_popover.hbs";
+import render_compose_select_enter_behaviour_popover from "../templates/popovers/compose_select_enter_behaviour_popover.hbs";
+import render_mobile_message_buttons_popover from "../templates/popovers/mobile_message_buttons_popover.hbs";
 
 import * as channel from "./channel";
 import * as common from "./common";
diff --git a/web/src/emoji_picker.js b/web/src/emoji_picker.js
index d09b0f71a4..971782e835 100644
--- a/web/src/emoji_picker.js
+++ b/web/src/emoji_picker.js
@@ -2,10 +2,10 @@ import $ from "jquery";
 
 import emoji_codes from "../../static/generated/emoji/emoji_codes.json";
 import * as typeahead from "../shared/src/typeahead";
-import render_emoji_popover from "../templates/emoji_popover.hbs";
-import render_emoji_popover_emoji_map from "../templates/emoji_popover_emoji_map.hbs";
-import render_emoji_popover_search_results from "../templates/emoji_popover_search_results.hbs";
-import render_emoji_showcase from "../templates/emoji_showcase.hbs";
+import render_emoji_popover from "../templates/popovers/emoji/emoji_popover.hbs";
+import render_emoji_popover_emoji_map from "../templates/popovers/emoji/emoji_popover_emoji_map.hbs";
+import render_emoji_popover_search_results from "../templates/popovers/emoji/emoji_popover_search_results.hbs";
+import render_emoji_showcase from "../templates/popovers/emoji/emoji_showcase.hbs";
 
 import * as blueslip from "./blueslip";
 import * as compose_ui from "./compose_ui";
@@ -646,9 +646,9 @@ function get_default_emoji_popover_options() {
             emoji_popover_instance = instance;
             const $popover = $(instance.popper);
             $popover.addClass("emoji-popover-root");
-            instance.setContent(ui_util.parse_html(
-                generate_emoji_picker_content(current_message_id),
-            ));
+            instance.setContent(
+                ui_util.parse_html(generate_emoji_picker_content(current_message_id)),
+            );
             emoji_catalog_last_coordinates = {
                 section: 0,
                 index: 0,
diff --git a/web/src/message_actions_popover.js b/web/src/message_actions_popover.js
index 00dbe0b0d3..8c90e0fc2a 100644
--- a/web/src/message_actions_popover.js
+++ b/web/src/message_actions_popover.js
@@ -1,7 +1,7 @@
 import ClipboardJS from "clipboard";
 import $ from "jquery";
 
-import render_actions_popover from "../templates/actions_popover.hbs";
+import render_actions_popover from "../templates/popovers/actions_popover.hbs";
 
 import * as blueslip from "./blueslip";
 import * as compose_actions from "./compose_actions";
diff --git a/web/src/playground_links_popover.js b/web/src/playground_links_popover.js
index dadfceee20..aa7f4bab96 100644
--- a/web/src/playground_links_popover.js
+++ b/web/src/playground_links_popover.js
@@ -1,7 +1,7 @@
 import $ from "jquery";
 import url_template_lib from "url-template";
 
-import render_playground_links_popover from "../templates/playground_links_popover.hbs";
+import render_playground_links_popover from "../templates/popovers/playground_links_popover.hbs";
 
 import * as blueslip from "./blueslip";
 import * as popover_menus from "./popover_menus";
diff --git a/web/src/scheduled_messages_popover.js b/web/src/scheduled_messages_popover.js
index 656b87384d..e41a12c99f 100644
--- a/web/src/scheduled_messages_popover.js
+++ b/web/src/scheduled_messages_popover.js
@@ -1,9 +1,9 @@
 import $ from "jquery";
 import {delegate} from "tippy.js";
 
+import render_send_later_popover from "../templates/popovers/send_later_popover.hbs";
 import render_send_later_modal from "../templates/send_later_modal.hbs";
 import render_send_later_modal_options from "../templates/send_later_modal_options.hbs";
-import render_send_later_popover from "../templates/send_later_popover.hbs";
 
 import * as compose from "./compose";
 import * as compose_validate from "./compose_validate";
diff --git a/web/src/user_card_popover.js b/web/src/user_card_popover.js
index 9d64183a09..4da52e5fe8 100644
--- a/web/src/user_card_popover.js
+++ b/web/src/user_card_popover.js
@@ -4,9 +4,9 @@ import $ from "jquery";
 import tippy from "tippy.js";
 
 import render_confirm_mute_user from "../templates/confirm_dialog/confirm_mute_user.hbs";
-import render_user_card_popover from "../templates/user_card_popover.hbs";
-import render_user_card_popover_avatar from "../templates/user_card_popover_avatar.hbs";
-import render_user_card_popover_manage_menu from "../templates/user_card_popover_manage_menu.hbs";
+import render_user_card_popover from "../templates/popovers/user_card/user_card_popover.hbs";
+import render_user_card_popover_avatar from "../templates/popovers/user_card/user_card_popover_avatar.hbs";
+import render_user_card_popover_manage_menu from "../templates/popovers/user_card/user_card_popover_manage_menu.hbs";
 
 import * as blueslip from "./blueslip";
 import * as buddy_data from "./buddy_data";
diff --git a/web/src/user_group_popover.js b/web/src/user_group_popover.js
index 68e8006801..c04b547717 100644
--- a/web/src/user_group_popover.js
+++ b/web/src/user_group_popover.js
@@ -1,6 +1,6 @@
 import $ from "jquery";
 
-import render_user_group_info_popover from "../templates/user_group_info_popover.hbs";
+import render_user_group_info_popover from "../templates/popovers/user_group_info_popover.hbs";
 
 import * as blueslip from "./blueslip";
 import * as buddy_data from "./buddy_data";
diff --git a/web/src/user_topic_popover.js b/web/src/user_topic_popover.js
index 0f4ab3c094..6d9198159a 100644
--- a/web/src/user_topic_popover.js
+++ b/web/src/user_topic_popover.js
@@ -1,6 +1,6 @@
 import $ from "jquery";
 
-import render_change_visibility_policy_popover from "../templates/change_visibility_policy_popover.hbs";
+import render_change_visibility_policy_popover from "../templates/popovers/change_visibility_policy_popover.hbs";
 
 import * as popover_menus from "./popover_menus";
 import * as popover_menus_data from "./popover_menus_data";
diff --git a/web/templates/compose_control_buttons.hbs b/web/templates/compose_control_buttons.hbs
index f9cbbc75d9..782f999213 100644
--- a/web/templates/compose_control_buttons.hbs
+++ b/web/templates/compose_control_buttons.hbs
@@ -24,7 +24,7 @@
     </div>
     <div class="divider hide-sm show-md hide-mc">|</div>
     <div class="{{#if message_id}}hide-lg{{else}}hide-sm show-md hide-mc{{/if}}">
-        {{> compose_control_buttons_in_popover}}
+        {{> popovers/compose_control_buttons/compose_control_buttons_in_popover}}
     </div>
     <a role="button" class="compose_control_button compose_draft_button hide-sm" tabindex=0 href="#drafts" data-tooltip-template-id="compose_draft_tooltip_template">
         {{t 'Drafts' }}
diff --git a/web/templates/actions_popover.hbs b/web/templates/popovers/actions_popover.hbs
similarity index 100%
rename from web/templates/actions_popover.hbs
rename to web/templates/popovers/actions_popover.hbs
diff --git a/web/templates/change_visibility_policy_popover.hbs b/web/templates/popovers/change_visibility_policy_popover.hbs
similarity index 100%
rename from web/templates/change_visibility_policy_popover.hbs
rename to web/templates/popovers/change_visibility_policy_popover.hbs
diff --git a/web/templates/compose_control_buttons_in_popover.hbs b/web/templates/popovers/compose_control_buttons/compose_control_buttons_in_popover.hbs
similarity index 100%
rename from web/templates/compose_control_buttons_in_popover.hbs
rename to web/templates/popovers/compose_control_buttons/compose_control_buttons_in_popover.hbs
diff --git a/web/templates/compose_control_buttons_popover.hbs b/web/templates/popovers/compose_control_buttons/compose_control_buttons_popover.hbs
similarity index 100%
rename from web/templates/compose_control_buttons_popover.hbs
rename to web/templates/popovers/compose_control_buttons/compose_control_buttons_popover.hbs
diff --git a/web/templates/compose_select_enter_behaviour_popover.hbs b/web/templates/popovers/compose_select_enter_behaviour_popover.hbs
similarity index 100%
rename from web/templates/compose_select_enter_behaviour_popover.hbs
rename to web/templates/popovers/compose_select_enter_behaviour_popover.hbs
diff --git a/web/templates/emoji_popover.hbs b/web/templates/popovers/emoji/emoji_popover.hbs
similarity index 100%
rename from web/templates/emoji_popover.hbs
rename to web/templates/popovers/emoji/emoji_popover.hbs
diff --git a/web/templates/emoji_popover_emoji.hbs b/web/templates/popovers/emoji/emoji_popover_emoji.hbs
similarity index 100%
rename from web/templates/emoji_popover_emoji.hbs
rename to web/templates/popovers/emoji/emoji_popover_emoji.hbs
diff --git a/web/templates/emoji_popover_emoji_map.hbs b/web/templates/popovers/emoji/emoji_popover_emoji_map.hbs
similarity index 100%
rename from web/templates/emoji_popover_emoji_map.hbs
rename to web/templates/popovers/emoji/emoji_popover_emoji_map.hbs
diff --git a/web/templates/emoji_popover_search_results.hbs b/web/templates/popovers/emoji/emoji_popover_search_results.hbs
similarity index 100%
rename from web/templates/emoji_popover_search_results.hbs
rename to web/templates/popovers/emoji/emoji_popover_search_results.hbs
diff --git a/web/templates/emoji_showcase.hbs b/web/templates/popovers/emoji/emoji_showcase.hbs
similarity index 100%
rename from web/templates/emoji_showcase.hbs
rename to web/templates/popovers/emoji/emoji_showcase.hbs
diff --git a/web/templates/left_sidebar_stream_setting_popover.hbs b/web/templates/popovers/left_sidebar_stream_setting_popover.hbs
similarity index 100%
rename from web/templates/left_sidebar_stream_setting_popover.hbs
rename to web/templates/popovers/left_sidebar_stream_setting_popover.hbs
diff --git a/web/templates/mobile_message_buttons_popover.hbs b/web/templates/popovers/mobile_message_buttons_popover.hbs
similarity index 100%
rename from web/templates/mobile_message_buttons_popover.hbs
rename to web/templates/popovers/mobile_message_buttons_popover.hbs
diff --git a/web/templates/playground_links_popover.hbs b/web/templates/popovers/playground_links_popover.hbs
similarity index 100%
rename from web/templates/playground_links_popover.hbs
rename to web/templates/popovers/playground_links_popover.hbs
diff --git a/web/templates/send_later_popover.hbs b/web/templates/popovers/send_later_popover.hbs
similarity index 100%
rename from web/templates/send_later_popover.hbs
rename to web/templates/popovers/send_later_popover.hbs
diff --git a/web/templates/user_card_popover.hbs b/web/templates/popovers/user_card/user_card_popover.hbs
similarity index 98%
rename from web/templates/user_card_popover.hbs
rename to web/templates/popovers/user_card/user_card_popover.hbs
index d49b0dca09..9a066dbb1e 100644
--- a/web/templates/user_card_popover.hbs
+++ b/web/templates/popovers/user_card/user_card_popover.hbs
@@ -52,7 +52,7 @@
             <li>{{ user_type }}</li>
         {{/if}}
         {{!-- Display selected custom profile fields in this popover. --}}
-        {{> user_custom_profile_fields profile_fields=display_profile_fields for_user_card_popover=true}}
+        {{> ../../user_custom_profile_fields profile_fields=display_profile_fields for_user_card_popover=true}}
 
         <li class="only-visible-for-spectators">{{t "Joined {date_joined}" }}</li>
 
diff --git a/web/templates/user_card_popover_avatar.hbs b/web/templates/popovers/user_card/user_card_popover_avatar.hbs
similarity index 100%
rename from web/templates/user_card_popover_avatar.hbs
rename to web/templates/popovers/user_card/user_card_popover_avatar.hbs
diff --git a/web/templates/user_card_popover_manage_menu.hbs b/web/templates/popovers/user_card/user_card_popover_manage_menu.hbs
similarity index 100%
rename from web/templates/user_card_popover_manage_menu.hbs
rename to web/templates/popovers/user_card/user_card_popover_manage_menu.hbs
diff --git a/web/templates/user_group_info_popover.hbs b/web/templates/popovers/user_group_info_popover.hbs
similarity index 100%
rename from web/templates/user_group_info_popover.hbs
rename to web/templates/popovers/user_group_info_popover.hbs
diff --git a/web/tests/i18n.test.js b/web/tests/i18n.test.js
index f6dcd7f27d..eee7eb78d3 100644
--- a/web/tests/i18n.test.js
+++ b/web/tests/i18n.test.js
@@ -77,12 +77,12 @@ run_test("t_tag", ({mock_template}) => {
             "http://zulip.zulipdev.com/#narrow/stream/101-devel/topic/testing/near/99",
     };
 
-    mock_template("actions_popover.hbs", true, (data, html) => {
+    mock_template("popovers/actions_popover.hbs", true, (data, html) => {
         assert.equal(data, args);
         assert.ok(html.indexOf("Citer et répondre") > 0);
     });
 
-    require("../templates/actions_popover.hbs")(args);
+    require("../templates/popovers/actions_popover.hbs")(args);
 });
 
 run_test("tr_tag", ({mock_template}) => {